Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm2 (to 5 mm/mm2).
EXTANT SEED PLANTS/SPERMATOPHYTA
Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and PHYA/PHYCgene pairs.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood 0; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: myricetin, delphinidin scattered, asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, "C" with a single trace; A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; palaeohexaploidy [gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
Evolution. Divergence & Distribution. Divergence may begin in the Albian 111-104 m.y.a. (Wikström et al. 2001) or 116-114 m.y.a. (Anderson et al. 2005). Magallón and Castillo (2009) estimated ca 110.7 and 111.3 m.y. for relaxed and constrained penalized likelihood ages, Moore et al. (2010: 95% HPD) proposed a somewhat younger (104-)100(-95) m.y. age.
Ecology & Physiology. There is a variety of companion cell morphologies in the phloem. Transfer cells, companion cells with few plasmodesmata but numerous wall ingrowths, and intermediary cells, characterized by having numerous plasmodesmata that branch in the outer part of the walls adjacent to the bundle sheath cells, seem to be notably common in taxa found in this part of the tree (Turgeon et al. 2001; Turgeon 2010: Santalales and Berberidopsidales i.a. not included in study, see also Fabaceae, etc.). There seems to be a correlation between the presence of intermediary cells (see especially Lamiales) and the presence of raffinose and stachyose in the translocate, and active phloem loading of sugars is to be expected with such companion cell morphologies. This has a number of physiological consequences, while also keeping mesophyll tissue low in sugars that might otherwise attract and/or benefit herbivores (Turgeon 2010).
Phylogeny. See the Dilleniales page for discussion on the relationships of these groups, which have no firm position as yet, although it is increasingly likely that Caryophyllales are close - perhaps even sister - to the asterids, whether (e.g. Bell et al. 2010) or not Dilleniales are sister to Caryophyllales.
CARYOPHYLLALES Berchtold & J. Presl Main Tree, Synapomorphies.
(Odd ecology and/or physiology); plant often not mycorrhizal; root hair cells in vertical files [sampling!]; (tracheids +); (cork pericyclic); perforation plates not bordered; only alternate vascular pitting; scanty vasicentric parenchyma; both uni- and multiseriate rays present; lamina margins entire; anther wall with outer secondary parietal cell layer developing directly into the endothecium, inner secondary parietal layer dividing; pollen colpate, tectum spinulose; G , when G = K or P, opposite them, style branches long; ovules with outer integument 2-3(-4) cells across, innner integument 2(-3) cells across; fruit a loculicidal capsule; seed testal; embryo long. - 34 families, 811 genera, 11510 species.
Note: Possible apomorphies are now being added throughout the site; they are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because there is very considerable homoplasy for many characters, with with variation within and between clades. Furthermore, basic information for all too many characters is very incomplete, often coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...
Evolution. Divergence & Distribution. Caryophyllales contain ca 6.3% of eudicot diversity (Magallón et al. 1999).
Crown group divergence may have begun 90-83 m.y.a. (Wikström et al. 2001); Anderson et al. (2005: Rhabdodendraceae also included) suggests figures of 102-99 m.y., while Moore et al. (2010: 95% HPD, only two taxa included) estimate a mere (71-)67(-63) m.y., Magallón and Castillo (2009) ca 94.35 m.y.. X. Wang (2010a: p. 22) inclines to the idea that Caryophyllales represent a very ancient clade: "Caryophyllales should represent, or at least is close to, the most primitive angiosperms". He compared their flowers with reproductive structures of the conifer Voltziales. Less spectacularly, Doyle (2012) suggested that tricolpate pollen was "retained" in Caryophyllales.
Ecology & Physiology. Many families are tolerant of saline/arid conditions, and the order is notable for the number of taxa than are halophytes, tolerating salt concentrations of 200mM (Flowers & Colmer 2008; Flowers er al. 2010), or that have a distinctive habit (e.g. climbers with grapnel organs) or physiology (carnivory, C4 pathway, CAM) or both. Perhaps associated with this, Lee et al. (2011) found that genes involved in metabolic processes involving sulphur compounds clustered at this node. It is noteworthy that sulphated phenolic compounds are also found in seagrasses (McMillan et al. 1980); here they occur in the [[Frankeniaceae + Tamaricaceae] [Plumbaginaceae + Polygonaceae]] part of the tree in particular, and the plants with such compounds are often halophytic.
Plant-Animal Interactions. Some chrysomelid beetles - Alticinae, Cassidinae-Hispinae - seem notably more common on this clade than others (Jolivet & Hawkeswood 1995).
Bacterial/Fungal Associations. Landis et al. (2002) and Trappe (1987) suggested that both Polygonales and Caryophyllales (here just the one order) commonly lacked mycorrhizae, although there are some exceptions (e.g. some Nyctaginaceae and Amaranthaceae).
Purple-spored smuts and Uromyces rusts parasitize several families, including Plumbaginaceae, Polygonaceae and core Caryophyllales (Savile 1979b: he considered this to be a strong sign that the groups were close).
Chemistry, Morphology, etc. Cuénoud (2002a, b) summarizes variation in the order. There are many unusual characters here, but their phylogenetic significance is unclear, partly because of sampling problems; e.g. knowledge of anther wall development is poor (Dahlgren & Clifford 1982). Furthermore, members of the basal pectinations in the clade immediately below core Caryophyllales are particularly poorly known. Given the variation in carpel number in the clade, it is with some hesitation that three carpels is suggested as the plesiomorphic condition.
Isoflavonoids are scattered in the group (Mackova et al. 2006), perhaps especially in the core Caryophyllales. Flavonol sulphates occur in Plumbaginaceae, Polygonaceae, and Amaranthaceae (Chenopodiaceae s. str.), and sulphated betalains in Phytolaccaceae.
For root hair development, see Dolan and Costa (2001). Carlquist (2010) suggests that few families in Caryophyllales have "truly adult" wood patterns. Placement of several features of wood anatomy on the tree need checking, although Carlquist (e.g. 2002b, 2003a, 2010) provided a vast amount of detail (see also Core Caryophyllales). Non-bordered perforation plates may be a synapomorphy for Caryophyllales or Caryophyllales and Santalales (Carlquist 2000a; see also Carlquist 2010). Anomalous secondary thickening by successive cambia is widespread, often occurring in lianes, and there is considerable variation in the morphology of these cambia (Carlquist 2010, much discussion), and maximally biseriate rays are also widespread (an in Asteropeiaceae, but not core Caryophyllales - Nandi et al. 1998). Similarities in sieve tube plastids between Triplarieae (Polygonaceae) and core Caryophyllales are here treated as parallelisms (c.f. Judd & Olmstead 2004).
The outer stamens are often initiated in pairs, especially in core Caryophyllales, but also elsewhere in the order (Ronse Decraene & Smets 1993). A petal and adjacent (antepetalous) stamen are developmental units in Plumbaginaceae and Caryophyllaceae (Friedrich 1956; Ronse Decraene et al. 1998). Trinucleate pollen is common. Carpels that are open in development are known both from Polygonaceae and core Caryophyllales (Tucker & Kantz 2001). The rpl23 gene is a pseudogene in the few Caryophyllales examined (Logacheva et al. 2008).
It is unclear where the character of starchy endosperm is to be put on the tree. The condition is unfortunately not known for taxa in the pectinations just below core Caryophyllales. Netolitzky (1926) noted that taxa here included in core Caryophyllales lacked starchy endosperm, and starch was not recorded from the thin endosperm found in the seeds of some Amaranthaceae (Shepherd et al. 2005b and references), but Narayana and Lodha (1963) reported starch in the young endosperm of Orygia (and Corbichonia: Lophiocarpaceae) and Kajale (1954) in the endosperm of Rivina humilis (Phytolaccaceae). Although in the Flora of China several families of core Caryophyllales are reported to have starchy endosperm (e.g. Dequan & Gilbert 2003), these must be mistakes for the perisperm, which is starchy, the nature ofr endosperm reserves in the Rhabdodendraceae to Cactaceae clade is apparently an open issue. Below it is placed as an apomorphy for the Droseraceae to Polygonaceae clade.
Phylogeny. Hilu et al. (2003: matK analysis alone) suggest that Caryophyllales are sister to Asterids, a relationship that has been found in some other studies (e.g. Soltis et al. 1997, c.f. also Nandi et al. 1998). A relationship between Caryophyllales and Dilleniales has also been suggested (D. Soltis et al. 2003a), see below for more details. However, Caryophyllales alone (or perhaps with Santalales) now seem to be sister to the asterids, although the support is still only moderate; see the Dilleniales page for further discussion.
Within Caryophyllales, Rhabdodendraceae were sister to the other members in an early rbcL analysis of Fay et al. (1997b) and in the Bayesian analysis of Soltis et al. (2007a). Cuénoud et al. (2002) found that Simmondsia was grouped with Rhabdodendron in a matK analysis, but with only weak support, but in two- and four-gene analyses (with poorer sampling) it was associated with core Caryophyllales; in trees shown by Drysdale et al. (2007) and Brockington et al. (2007, esp. 2009) a position of Rhabdodendron as sister to the rest of core Caryophyllales was again found in most analyses, and is adopted here (see also Soltis et al. 2011). Hilu et al. (2003: matK analysis alone) also suggested relationships between Rhabdodendraceae and this part of the tree.
There are two main groups within Caryophyllales, the core Caryophyllales, the old Centrospermae, and four small families associated with them, and Polygonaceae, etc. This latter clade, including Plumbaginaceae, Polygonaceae, Nepenthaceae, and Droseraceae, is well-supported (Morton et al. 1997b; Soltis et al. 2011), although it was not recovered in the mitochondrial analysis of Qiu et al. (2010: support low). It includes four carnivorous families (see also Albert et al. 1992; Meimberg et al. 2000; Cuénoud et al. 2002; Cameron et al. 2002; Renner & Specht 2010) and other families with distinctive vegetative morphologies (see also Heubl et al. 2006). Within the other major clade, Asteropeiaceae and Physenaceae form a well supported pair, in turn showing a well-supported sister group relationship to core Caryophyllales (Källersjö et al. 1998). Similarly, Asteropeiaceae and Simmondsiaceae, the only two taxa from this part of the order that were included, were successively sister groups to the core (D. Soltis et al. 2000). The tree below is based largely on those presented by Meimberg et al. (2000), Cameron et al. (2002: 4 genes) and Cuénoud et al. (2002: matK alone). For relationships within the core Caryophyllales, which are poorly understood, see below.
Previous Relationships. Takhtajan's (1997) Plumbaginanae are monotypic; Nepenthanae included Droseraceae and some other Caryophyllales, but also families now in Ericales, etc. Many of the families in Caryophyllales were included in Cronquist's (1981) Caryophyllidae. Plumbaginaceae are rather similar in a few respects to Primulaceae and relatives and the two had been considered close (see Cronquist 1981 for discussion); Friedrich (1956) had effectively discounted such ideas.
Includes Achatocarpaceae, Aizoaceae, Amaranthaceae, Anacampserotaceae, Ancistrocladaceae, Asteropeiaceae, Barbeuiaceae, Basellaceae, Cactaceae, Caryophyllaceae, Didiereaceae, Dioncophyllaceae, Droseraceae, Drosophyllaceae, Frankeniaceae, Gisekiaceae, Halophytaceae, Hypertelis, Limeaceae, Lophiocarpaceae, Macarthuria, Microteaceae, Molluginaceae, Montiaceae, Nepenthaceae, Nyctaginaceae, Physenaceae, Phytolaccaceae, Plumbaginaceae, Polygonaceae, Portulacaceae, Rhabdodendraceae, Sarcobataceae, Simmondsiaceae, Stegnospermataceae, Talinaceae, Tamaricaceae.
Synonymy: Aizoineae Doweld, Basellineae Doweld, Cactineae Bessey, Caryophyllineae Bessey, Chenopodiineae Engler, Nyctaginineae Doweld, Phytolaccineae Engler, Portulacineae Doweld, Simmondsiineae Reveal, Stegnospermatineae Doweld - Aizoales Boerlage, Alsinales J. Presl, Amaranthales Berchtold & J. Presl, Ancistrocladales Reveal, Atriplicales Horaninow, Cactales Berchtold & J. Presl, Chenopodiales Berchtold & J. Presl, Dioncophyllales Reveal, Droserales Berchtold & J. Presl, Frankeniales Link, Illecebrales Berchtold & J. Presl, Mesembryanthemales Link, Nepenthales Dumortier, Nyctaginales Berchtold & J. Presl, Opuntiales Willkom, Paronychiales Link, Petiveriales Link, Physenales Takhtajan, Phytolaccales Link, Plumbaginales Berchtold & J. Presl, Polygonales Berchtold & J. Presl, Portulacales Berchtold & J. Presl, Reaumuriales Martius, Rhabdodendrales Doweld, Riviniales Martius, Scleranthales Link, Silenales Lindley, Simmondsiales Reveal, Staticales Link, Stellariales Dumortier, Tamaricales Link, Telephiales Link - Caryophyllanae Takhtajan, Nepenthanae Reveal, Plumbaginanae Reveal, Polygonanae Reveal, Rhabdodendranae Doweld, Simmondsianae Doweld - Caryophyllidae Takhtajan, Plumbaginidae C. Y. Wu, Polygonidae C. Y. Wu - Amaranthopsida Horaninov, Cactopsida Brogniart, Caryophyllopsida Bartling, Opuntiopsida Endlicher, Polygonopsida Brongniart, Plumbaginopsida Endlicher
[[Droseraceae [Nepenthaceae [Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]]] [[Frankeniaceae + Tamaricaceae] [Plumbaginaceae + Polygonaceae]]]: acetogenic naphthoquinones +; pit glands +; endosperm starchy.
Evolution. Divergence & Distribution. The two main groups in this clade diverged perhaps 82-76 m.y.a. (Wikström et al. 2001).
For gland morphology and vascularization in this part of the tree, see Renner and Specht (2011); optimisation is not easy.
Chemistry, Morphology, etc. For the vegetative morphology of carnivorous members of this clade, see Kaplan (1997, vol. 2,: chap. 18). The acetogenic naphthoquinone plumbagin is known from Plumbaginaceae, Droseraceae, Nepenthaceae, and Dioncophyllaceae, and related compounds are found in Polygonaceae (Culham & Gornall 1994; Kovácik & Repcák 2006).
[Droseraceae [Nepenthaceae [Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]]]: plumbagin +; plants carnivorous [insectivorus]; vascularized multicellular stalked or sessile glands +; inflorescence ± cymose; C contorted; anthers extrorse, dorsifixed; ovary unilocular.
Evolution. Ecology & Physiology. The acquisition of carnivory may have happened more than once in this clade, or it occurred once and then was lost, perhaps more likely given the topologies found (Meimberg et al. 2000; Cameron et al. 2002: see also Schlauer 1997). Renner and Specht (2011) suggest scenarios for the evolution of digestive glands, and find that novel chitinase genes - otherwise involved in anti-fungal activities - have evolved in this group in the context of the extracellular degradation of the chitin of arthropods (Renner & Specht 2012).
Heubl et al. (2006) suggest that fly-paper traps are the plesiomorphic condition for the group, but note that where features like this or the possession of circinate leaves and pollen tetrads are placed on the tree will depend on the mode of character optimisation used.
Chemistry, Morphology, etc. Heubl and Wistuba (1997) suggested that both Droseraceae and Nepenthaceae had ploidy levels of 8 or 16, based on x = 5 or thereabouts.
For information on acetogenic quinones and alkaloids, see Hegnauer (1986), Bringmann and Pokorny (1995) and Bentley (1998), for carnivory, see Lloyd (1942) and Juniper et al. (1989), and for general information, especially photographs, see McPherson (2010).
Phylogeny. Metcalfe (1952a) suggested relationships between members of this group based on anatomical similarities. Williams et al. (1994) drew atttention to possible relationships between Dioncophyllaceae and Drosophyllum in particular, and Drosophyllum and Nepenthaceae were also found to be weakly associated (Morton et al. 1997b). Soltis et al. (2011) found Drosera and Nepenthes to be sister taxa, but the support was only moderate and sampling not extensive. For detailed relationships, see Meimberg et al. (2000) and Cameron et al. (2002); Drosophyllaceae are sister to Dioncophyllaceae + Ancistrocladaceae, with good support, in an analysis of matK sequences, the position of Nepenthaceae being uncertain (Cuénoud et al. 2002). For a synapomorphy scheme for the whole group, see in part Albert and Stevenson (1996) and Meimberg et al. (2000: the floral characters listed are mostly plesiomorphies), but especially Heubl et al. (2006).
DROSERACEAE Salisbury, nom. cons. Back to Caryophyllales
Rosette herbs, (woody; climbers); flavonols, ellagic acid +; cork?; young stem with separate bundles in one or two rings, medullary rays broad; cambium 0; (medullary bundles +); nodes 1:1; petiole bundles various; stomata also tetracytic or actinocytic; pit glands 0, vascularized glands with xylem only; leaves adaxially circinate, long-stalked glands or trigger hairs adaxial, leaf moves, stipules +, intrapetiolar, or 0; inflorescence terminal, cyme monochasial, (bracts/bracteoles 0); K often connate at base, C ± marcescent; stamens = and opposite sepals (-15 - Dionaea), (introrse), (connective expanded); (tapetum amoeboid); pollen in tetrads, bi- or trinucleate, 3-multiporate, pores equatorial, protrusions along the borders of adjoining grains, operculate or not, (with orbicules); G [3(-5)], median member abaxial, styles separate, often bifid, (style connate - Dionaea), stigmas expanded, papillate; placentation parietal (basal - Dionaea); ovules 3-many/carpel, parietal tissue often absent, nucellar epidermal cells enlarged ["nucellar endothelium"], (column of cells in nucellus), ; embryo sac haustorium +; (fruit indehiscent); exotesta palisade or not, (endotesta with U thickenings), endotegmic cells small, ± sclerotic, or mucilaginous; endosperm nuclear, (embryo short); (germination cryptocotylar; cotyledons 0); n = 5, 5-17, 19, chromosomes 1.5³ µm (<6µm [Dionaea]); chloroplast rpl2 intron 0 [one species!].
3[list]/115: Drosera (110). World-wide (map: from Hultén 1971; Fl. Austral. 8. 1982; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Correa A. & Silva 2005). [Photos - Collection, Collection.]
Evolution. Divergence & Distribution. The beginning of diversification within Drosera may date to ca 42 m.y.a., although a pre-continental drift time has also been suggested (Yesson & Culham 2006 and references). Drosera is exceptionally diverse in S.W. Australia, which has about one third of the species in the whole genus; diversification may be linked to the onset of the Mediterranean climate there some 15-10 m.y.a. The Australian pygmy sundews include D. meristocaulis, a plant from Guyana (Rivadavia et al. 2012).
Ecology & Physiology. Aldrovandra and Dionaea both have snap-traps with multicellular trigger hairs, etc. (Cameron et al. 2002). The traps of Dionaea close in about 100 ms, the movement being aided by the leaf blades changing from concave to convex (Forterre et al. 2005), while in the snap traps of Aldrovanda the blade does not change shaps, but the midrib does (Poppinga & Joyeux 2011); Volkov et al. (2008) and Escalante-Pérez et al. (2011) provide details of the physiological mechanisms involved in the former genus. Gibson and Waller (2009; see also Williams 2002) discuss the evolution of the snap traps of Dionaea, which are unique in angiosperms; it is perhaps associated with the capture of larger prey than the plant could otherwise utilize.
Indeed, there is quite a variety of different hair types in Drosera itself, and some of these may be comparable with the marginal spines of Dionaea (Hartmeyer & Hartmeyer 2010; Hartmeyer et al. 2013)). Thus the leaves of Drosera glanduligera have rapidly-moving eglandular marginal hairs that can snap tight in as little at 75 ms and that pin the prey against glandular hairs in the centre of the blade (Poppinga et al. 2012). The glands of at least some species of Drosera produce a ribonuclease which may aid the plant in obtaining phosphorous from its prey, and perhaps also in defence against viruses (Okabe et al. 2005). For further literature, see Peroutka et al. (2008b).
Chemistry, Morphology, etc. Metcalfe and Chalk (1950) describe distinctive vascular patterns in the inflorescence axis and petiole. I(n Drosera aliciae young inflorescences (before flower buds are evident) appear to have abaxially circinate vernation, but this is probably a reflection of the way the monochasial cyme is developing.
The pollen of Droseraceae is remarkable. When the pollen is hydrated, there are protrusions along the borders of adjoining grains, and it Dionaea and Drosera regia these protrusions persist in the dehydrated state and are operculate (Halbritter et al. 2012). Clarification of the phylogeny in the family is in order (see below).
See Hegnauer (1966, 1989) for chemistry, Boesewinkel (1989) for ovule and seed anatomy, Hoshi and Kondo (1998) for chromosomes, Cutler and Gregory (1998) for general anatomy, Conran et al. (2007) for gland morphology, Pace (1912) for embryology, and Le Maout and Decaisne (1868), Baillon (1887), Kubitzki (2002d), McPherson (2008), and the Carnivorous Plants Database for general information.
Phylogeny. Aldrovandra and Dionaea may be sister taxa; both have snap-traps, n = 6, etc. (Cameron et al. 2002; Rivadavia et al. 2003: little support for the relationship); see also Williams et al. (1994) for phylogeny. Rivadavia et al. (2003) discuss the phylogeny of Drosera. The position of D. regia is unclear; in both chromosome number and pollen morphology (it has operculate protrusions in the pollen) it is rather different from other species of Drosera; it may be sister to the rest of the genus, or even closer to other genera in the family.
Synonymy: Aldrovandaceae Nakai, Dionaeaceae Rafinesque
[Nepenthaceae [Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]]: fibriform vessel elements +; rays 1-2 cells wide; petiole bundle(s) surrounded by massive sclerenchymatous ring with embedded vascular bundles, wing bundles +; leaves abaxially circinate; anthers basifixed.
Chemistry, Morphology, etc. Heubl et al. (2006) place a character, "petiole with cortical vascular bundles" at this node - see above!
NEPENTHACEAE Dumortier, nom. cons. Back to Caryophyllales
Plant a liane, climbing by twining portion of leaves, (± a rosette); flavonols +, ellagic acid 0; cork pericyclic; (also medullary bundles +); SiO2 bodies +; (vessel elements with scalariform perforation plates); true tracheids +; large spirally-thickened cells in pith, pericycle, etc.; nodes 5-9:5-9; cortical bundles in stem +; petiole bundle arcuate; glands not vascularized, peltate glands +; leaves sessile, blade portion basal, then narrow twining portion, terminated by pitcher [epiascidiate], blade vernation involute, leaf base broad; plant dioecious, inflorescence a raceme, bracts and bracteoles 0; P +, (3-)4, decussate, large flat nectariferous glands adaxially; staminate flowers: A connate into a central column, (4-)8-25; pollen in tetrads, trinucleate, apertures indistinct; pistillode 0; carpellate flowers: staminodes?; G [(3-)4(-6)], placentation axile, style short, stigma broad, papillate; ovules many/carpel, bistomal, outer integument becoming very long, parietal tissue 1 cell across, chalazal projection +; seeds numerous, spindle-shaped, minute; chalaza with hair-pin bundle, exotesta with much thickened inner walls; endosperm +, nuclear; n = 40.
1[list]/90. Madagascar to New Caledonia (map: see Meimberg & Heubl 2006). [Photo - Leaf; Collection.]
Evolution. Divergence & Distribution. Nepenthes is known fossil as pollen from Europe in the Eocene (Krutzsch 1989).
For the biogeography of Nepenthes, see Meimberg and Heubl (2006). Some analyses suggest that the Malesian Nepenthes (including species from New Caledonia and Australia) are derived from a stock represented by the extant taxa found to the west of Malesia, but different relationships are suggested by different genes.
Ecology & Physiology. Pavlovic et al. (2007) discuss the physiology of lamina and trap (see also Mithöfer 2011 and references). The liquid in the tank tends to be acid, and contains enzymes from the plant (Peroutka et al. 2008b; Adlassnig et al. 2011), however, how insects are trapped in the pitchers has long been unclear. Nectar is produced by the pitchers and attracts insects. Recent work suggests that the rim (peristome) of the pitcher is extremely wettable, and insects may aquaplane when they step on it, falling in to the pitcher below where they die and get digested; only when the rim is dry can insects walk on it easily, but they still may get trapped when they walk on to the wax-covered inner pitcher walls (Bohn & Federle 2004). Interestingly, the ant Camponotus schmitzi lives in close association with Nepenthes bicalcarata, and this ant can run across even the wetted rim. For the fauna of the liquid in the pitchers, see Kitching (2000).
On the whole the pichers seem not to be very efficient at capturing insects (Joel 1988), and the traps may have other functions. It has recently been found that some species of Nepenthes with particularly large pitchers capture the faeces of tree shrews (Tupaia montana) as they feed from glands on the inner surfaces of the lids (Chin et al. 2010), and in other cases nutrients from litter in the trap may be taken up by the plant (Adlassnig et al. 2011 and references).
Although mimicry with flowers has sometimes been invoked as an explanation of the distinctively coloured and shaped pitcher-rims, this is unlikely (Joel 1988; Ruxton & Schaefer 2011).
Chemistry, Morphology, etc. The expanded part of leaf is developed from the leaf base, as in many monocots, the twining petiole and the pitcher from the rest (e.g. Troll 1932); the leaf is epiascidiate.
The outer integument develops greatly after fertilisation and forms an exostome (Goebel 1933); there is a hair-pin bundle in the testa (Takhtajan 1988).
For general information, see Cheek and Jebb (2001: almost a monograph), Kubitzki (2002d), McPherson (2008) and the Carnivorous Plants Database, for chemistry, see Hegnauer (1966, 1990), for anatomy, Metcalfe (1952a) and Pant and Bhatnagar (1977), for the fauna of the pitchers, see Kitching (2000), and for the trapping of insects, see Bohn and Federle (2004: aquaplaning common).
Phylogeny. For relationships within Nepenthes, see Meimberg and Heubl (2006).
[Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]: ?
DROSOPHYLLACEAE Chrtek, Slavíkovà & Studnicka Back to Caryophyllales
Plant woody, small; chemistry?; cortical bundles in stem +, inverted; ?nodes; ?stomata; petiole bundles three, arcuate, inverted, sclerenchyma ring?; vascularized glands with xylem and phloem, pit glands 0; leaves linear, stalked glands abaxial, in lines, abaxially circinate, vernation revolute; flowers large, (C contorted), ± marcescent; A 10, attachment?; pollen trinucleate, tectate, pantoporate; G , opposite the K, placentation basal, styles separate, stigmas capitate; ovules several/carpel; fruit septicidal; seeds operculate, few; exotesta not palisade, endotesta crystalliferous, with U thickenings, exotegmen thick-walled; endosperm ?, embryo short; n = 6, chromosomes ³15 µm long; germination epigeal, ± cryptocotylar.
1/1: Drosophyllum lusitanicum. Southern Iberian Peninsula, Morocco (map: from Ortega et al. 1995). [Photos - Collection]
Evolution. Ecology & Physiology. For carnivory in Drosophyllum, see Plachno et al. (2009); the leaf produces a sweet (?attractive) scent. Although Drosophyllum looks quite delicate, it grows in very dry conditions and does not dry out fast; the mucilage on the tentacles is hygroscopic and may help the plant maintain a positive water balance (Adamec 2009).
Chemistry, Morphology, etc. Stem/leaf anatomy would repay investigation; both the cortical and petiole bundles appear to be inverted (Metcalfe & Chalk 1950, as Droseraceae). The flowers are relatively large; the stamens opposite the calyx are longest. Dehiscence of the fruit is down the ribs of the capsule and the valves are opposite the calyx.
For some anatomy, see Metcalfe (1952a), for ovule and seed, see Boesewinkel (1989), and for general information, see Kubitzki (2002d), McPherson (2008) and the Carnivorous Plants Database.
[Ancistrocladaceae + Dioncophyllaceae]: plants woody, lianes; ?mycorrhizae; (acetogenic napthyl isoquinoline alkaloids +); cork deep seated; petiole with inverted bundles in sclerenchyma ring; stomata actinocyclic; C contorted; A introrse.
Chemistry, Morphology, etc. For the distinctive napthyl isoquinoline alkaloids of the clade, see Bringmann (1986), Bringmann and Pokorny (1995), and Bringmann et al. (2008, and references); they are synthesised from polyketide precursors, not from aromatic amino acids, so are barely alkaloids in the strict sense. For growth patterns see Cremers (1974).
ANCISTROCLADACEAE Walpers, nom. cons. Back to Caryophyllales
Climbing by twining, with grapnels along one side of the branch opposite the leaves, not carnivorous; myricetin +, ellagic acid?; nodes 3:3; SiO2 bodies +; xylem parenchyma apotracheal, banded; cortex with with elongated pitted sclereids, sclereid band indistinct; petiole bundle annular; vascularized glands 0; lamina vernation supervolute, surface with glands [lepidote hairs in crypts]; flowers small, pedicels articulated; K quincuncial, (with abaxial glands), C contorted [?how common], basally connate; A (5) 10, whorl opposite petals larger, filaments broadened and ± connate basally and adnate to C; G [3(-4)], half or more inferior, style ± impressed into apex of ovary, long-branched, stigmas hippocrepiform or pinnatifid, ?type; ovule single [per flower], basal, hemitropous, outer integument "thick", ?nucellus; fruit a nut, K much enlarged; seed ruminate; exotesta "thin membranaceous"; endosperm cellular, embryo short; n = ?; seedling phanerocotylar, hypocotyl elongated.
1[list]/12. Tropical Africa to W. Borneo and Formosa (map: from van Steenis 1949a; Freson 1967; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011). [Photo - Fruits, Grapnels.]
Chemistry, Morphology, etc. 1/3 species tested had fluorescing wood. Minute stipules and flowers with four carpels are reported by Takhtajan (1997) and Porembski (2002). The pollen is like that of Dioncophyllaceae (Cronquist 1981).
For a little anatomy, see Metcalfe (1952a; more in van Tieghem 1903b), for chemistry, see Hegnauer (1989) and for general information, see Keng (1967a), Porembski (2002) and Heubl et al. (2010).
Previous Relationships. In the past Ancistrocladaceae have often been included in Theales or Theanae (Cronquist 1981; Takhtajan 1997).
DIONCOPHYLLACEAE Airy Shaw, nom. cons. Back to Caryophyllales
Climbing by recurved hooks on leaves, (shrubs); cyclopentenoid cyanogenic glycosides +, ellagic acid?; successive cambia +; xylem with included phloem; true tracheids +; wood parenchyma vasicentric or apotracheal-diffuse; nodes ?; cortex with massive band of fibrous tissue; petiole bundles 1-3, arcuate; (pit glands, vascularized glands 0); (first leaves linear, with stalked glands, adaxially circinate - Triphyophyllum), (leaves with parallel venation); K valvate or open; A 10-30; G [2, 5], placentation parietal, (connate style short), stigmas punctate, capitate (feathery - Triphyophyllum); ovules several/carpel, ?morphology, funicles long; capsule opening before maturity; seeds flattened, green when young, broadly winged; seed coat thick; endosperm ?nuclear, embryo with spreading semicircular cotyledons; n = 12, 18 [both Triphyophyllum peltatum]; germination epigeal, cryptocotylar.
3[list]/3. Tropical West Africa (map: from ; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
Evolution. Ecology & Physiology. The young plants of Triphyophyllum peltatum have some leaves that have a short blade and glandular hairs on the abaxial surface of the prolonged midrib (Green et al. 1979) - and they are abaxially circinate when young, just like the leaves of Drosophyllum, etc. It is at this stage that the plant may capture insects.
Chemistry, Morphology, etc. Androecial variation in Dioncophyllum is considerable - there may be five stamens opposite the petals, ten stamens, or ca 27 stamens... (Airy Shaw 1952).
For anatomy, see Metcalfe (1952a) and Miller (1975), for gross morphology, see Airy Shaw (1952), Gottwald and Parameswaran (1968) and Schmid (1964), for chemistry, Hegnauer (1966, as Flacourtiaceae, 1989) and Spencer and Siegler (1985), for carnivory, Bringmann et al. (2001), and for general information, see Porembski and Barthlott (2002), McPherson (2008: excellent photographs), and the Carnivorous Plants Database.
Classification. See Airy Shaw (1952).
Previous Relationships. See Airy Shaw (1952) for a summary. Dioncophyllales were included in Theanae by Takhtajan (1997).
[[Frankeniaceae + Tamaricaceae] [Plumbaginaceae + Polygonaceae]]: vessel elements with minute lateral wall pits +; sulphated flavonols, ellagic acid +; ovary 1-locular; outer and inner integuments 2-3 cells across; seed exotestal.
Chemistry, Morphology, etc. Sulphated phenolic compounds are common here; the plants with such compounds are often halophytic. Frankeniaceae, Tamaricaceae and Plumbaginaceae all have flat, multicellular glands of subepidermal origin (Conran et al. 2007). This is perhaps an apomorphy here (or still higher), with a loss in Polygonaceae; where to place this and other characters on the tree is difficult.
[Frankeniaceae + Tamaricaceae]: halophytic; bisulphated flavonols +, myricetin 0; wood storied; nodes ?; (rhomboidal crystals +); (stomatal orientation transverse); leaves small [<1 cm long], with salt-excreting glands; flowers small, 4-6-merous, C with basal adaxial appendages; pollen not spinulose; G with median member abaxial, placentation (intruded) parietal, (basal), style +, branched, stigmas capitate-clavate; fruit a loculicidal capsule; exotestal cells bulging or as hairs; endosperm +.
Evolution. Divergence & Distribution. It is equally parsimonious to assume that petal appendages are apomorphies for the family pair as it is to assume that they have evolved independently; in Tamaricaceae the Reamuria clade, members of which have these appendages, is sister to the rest of the family. Seeds with copious endosperm have the same distribution.
Chemistry, Morphology, etc. For salt glands, see Fahn (1979), for ovules, etc., see Mauritzon (1936b).
Phylogeny. The monophyly of the two families and their sister-group relationship have been confirmed by Gaskin et al. (2004).
Previous Relationships. Both Frankeniaceae and Tamaricaceae were placed in Violales by Cronquist (1981) and in Violanae by Takhtajan (1997), probably because of their parietal placentation.
FRANKENIACEAE Desvaux, nom. cons. Back to Caryophyllales
Herbs to shrubs; cork pericyclic or subepidermal; fibriform vessel elements +; wood rayless; cuticle wax crystalloids 0; leaves opposite, often ericoid; flowers also 7-merous, K connate, lobes induplicate-valvate, C clawed; A (3-)6(-24; inner whorl staminodial), slightly connate at the base or not, extrorse, versatile, tapetal cells binucleate; ?nectary; pollen trinucleate; G [(2-)3(-4)]; ovules (1-)2-6(-many)/carpel, parietal tissue 0, nucellar cap +, funicles long; exotestal cells large, papillate, papillae with terminal nail-like thickenings, endotestal cells thin-walled [?fibers], endotegmen with thick cuticle, tanniniferous; (polyembryony +), coenocytic micropylar endosperm haustorium +; n = 10, 15.
1/90. ± World-wide in warm, dry areas, but scattered (map: from Fl. Austral. 8. 1982; Whalen 1987; Jäger 1992; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase 2004). [Photos - Collection]
Chemistry, Morphology, etc. Some information is taken from Walia and Kapil (1965), Whalen (1987: taxonomy Old World Frankenia) and Olson et al. (2003: anatomy); for general accounts, see Surgis (1921) and and Kubitzki (2002d).
TAMARICACEAE Link, nom. cons. Back to Caryophyllales
Woody, also xeromorphic; (gypsum crystals +); cuticle waxes as tubes or curled rodlets; leaf bases often broad; inflorescence racemose (flowers solitary), bracteoles 0; K connate below or not, (C lacking appendages); stamens = or 2x C or more, most connate at base into 5 bundles, development centrifugal, anthers extrorse to introrse, variously attached; nectary ± disciform, with C and A on top, or inside or outside A (0); G [(2-)3-4(-5)], opposite petals, (style short), stigmas wet; ovules 2-many/carpel, parietal tissue 1-2 cells across; embryo sac tetrasporic [a variety of types, even in one species, often 16-nucleate bipolar]; seed with hairs at chalazal end, exotestal cells periclinally elongated and thick-walled, endotestal cells thin-walled, crystalliferous; endosperm usu. scanty, oil and protein as reserves, perisperm +, thin (0); n = (11) 12.
5[list]/90: Tamarix (55). Eurasia and Africa, esp. Mediterranean to Central Asia, commonly naturalised in North America (map: from Hultén & Fries 1986; Meusel et al. 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photos - Collection]
Chemistry, Morphology, etc. Reamuria is distinctive in having single terminal flowers, a contorted corolla, and basal adaxial scales on the petals, c.f. Frankeniaceae. It also has many centrifugal stamens arising from 10 primordia, it lacks a nectary, and its seeds have endosperm (Ronse Decraene 1990). The nucellus is very thin, the parietal cell not dividing.
See Joshi and Kajale (1936) and Johri and Kak (1954) for embryology, Hegnauer (1973, 1990) for chemistry, Czaja (1978) for seed storage, Zhang et al. (2001) for pollen and Gaskin (2002) for a general account.
Phylogeny. Relationships within the family are [[Holachna + Reamuria] [Myricaria + Tamarix]] (Gaskin et al. 2004). For a phylogeny of Myricaria, see Y. Wang et al. (2009).
Synonymy: Reamuriaceae Lindley
[Plumbaginaceae + Polygonaceae]: plants herbaceous; O-methylated flavonols, myricetin, quinones +; (SiO2 bodies +); (wood storeyed); cortical and/or medullary vascular bundles +; nodes 3:3; leaf base broad; pollen usu. starchy; G with median member adaxial; ovule single [per flower], basal; fruit surrounded by accrescent calyx which forms part of the dispersal unit; exotesta ± persistent, otherwise seed coat undistinguished; mitochondrial coxII.i3 intron 0.
Evolution. Plant-Animal Interactions. Lycaeninae caterpillars are quite commonly found on this family pair, probably because of the polyphenolics in their leaves (Fielder 1995).
Chemistry, Morphology, etc. For sterol composition in comparison to that of core Caryophyllales, see Wolfe et al. (1989), for anatomy, see Carlquist and Boggs (1996).
PLUMBAGINACEAE Jussieu, nom. cons. Back to Caryophyllales
Often salt tolerant; glycine betaine, choline-O-sulphate +, little oxalate accumulation; vascularized mucilage glands and epidermal glands +; cork subepidermal or cortical; secondary thickening odd; rays multiseriate; petiole bundles arcuate; cuticle wax crystalloids 0 (irregular platelets); stomata also paracytic; K connate, ribbed, C contorted; stamens = and opposite petals; pollen with irregular columellae, tectum continuous, itself with columellae, with rather coarse blunt spines; nectary on adaxial side of filament bases (elsewhere); G , stigmas capitate or not, (multicellular papillae +); ovule anatropous, parietal tissue 2-3 cells across, (nucellar cap ca 2 cells across - Plumbagella), funicle long and curled, obturator from wall at apex of ovary; embryo sac tetrasporic, 4-nucleate; endotegmen persistent; endosperm 4n or 5n, little persisting, embryo green.
27[list]/836 - three groups below. Predominantly Mediterranean to Central Asia, scattered elsewhere. [Photos - Collection]
1. Plumbaginoideae Burnett
Perennial herbs or shrubs; stems angled and striate; lamina (deeply lobed), petioles often short, (cauline stipules - Plumbago); inflorescence racemose, vegetative and reproductive shoots similar; (flowers heterostylous); K herbaceous, glandular, C (connate), lobes truncate-emarginate and then apiculate; style +, stigmatic receptive areas in bouquet-like aggregations along branch; fruit a basally circumscissile capsule, calyx herbaceous; n = 6, 7.
4/36. East Asia and Africa, Plumbago pantropical (map: from Baker 1948, probably over-optimistic, Plumbago in particular commonly cultivated).
2. Limonioideae Reveal
Plumbagin 0; lamina cartilaginous, with 5-10 marginal rows of whitish cells; C connate; stamens adnate to corolla; styles separate (single, branched), stigma capitate (filiform).
2A. Aegialitideae Peng
Shrublet; glycine betaine 0, ellagic acid +; successive cambia +; cortical vascular bundles +; branched sclereids +; lamina vernation involute, basal sheath surrounding stem; fruit?; n = ?
1/2. Indo-Malesian, Australia, in mangroves (map: from van Steenis 1949c, in blue).
Synonymy: Aegialitidaceae Linczewski
2B. Limonieae Reveal
Perennial herbs or shrubs; glycine betaines usu. 0, then beta-alanine betaines (and other quaternary ammonium compounds) +; leaves ± basal, (lamina margin deeply lobed), petioles often short; inflorescence capitate or branched, cymose, axis channelled, inflorescence leaves reduced or absent; (plant heterostylous); K scarious (also petal-like); pollen often dimorphic, columellae regular, tectum incomplete, reticulate; fruit an achene or circumscissile capsule; n = 8, 9; deletion of rpl16 intron.
22/800: Limonium (350), Acantholimon (165), Armeria (90: half on the Iberian Peninsula). Mostly Irano-Turanian (Mediterranean), but also S. Africa, S. South America, and W. Australia (map: from Hultén; Baker 1948; FloraBase 2004; Australia's Virtual Herbarium xii.2012, in red).
Synonymy: Armeriaceae Horaninow, Limoniaceae Seringe, nom. cons., Staticaceae Cassel
Evolution. Divergence & Distribution. Diversification in the family began perhaps as recently as 18-16 m.y.a. (Lledó et al. 2005). Limonieae are most diverse in the area from the western Mediterranean (Limonium, etc., with hybridization and hundreds of microspecies, some apomictic) to Central Asia (Acantholimon, etc.).
Ecology & Physiology. Members of the family prefer saline and sometimes rather dry conditions, and species of Limonium and some other Limonieae are succulent halophytes, the only members of the family that can grow in salt marshes (Hanson et al. 1994; Flowers & Colmer 2008; Ogburn & Edwards 2010). The quaternary ammonium compounds of one sort or another that have been found in practically all members of the family examined are involved in salt excretion, while choline O-sulphate may also be involved in sulphate detoxification (Hanson et al. 1994).
Pollination Biology & Seed Dispersal. In a number of Limonieae the calyx becomes scarious in fruit and helps in dispersal; in Plumbago the sticky calyx glands persist in fruit.
Chemistry, Morphology, etc. Glycine betaine is known from only a very few species of Limonium (and from Plumbago, etc.), but not from Aegalitis and Armeria and other Limonieae (Rhodes & Hanson 1993; Hanson et al. 1994); see Hanson et al. (1994) for choline-O-sulphate distribution.
For wood anatomy, which may be paedomorphic, the family perhaps having a more or less herbaceous ancestry, see Carlquist and Boggs (1996). There is extensive gross anatomical variation that probably can be integrated with the tribes/subfamilies - for example, there is a continuous ring of sclerenchyma outside the phloem in Plumbaginoideae, separate fascicles in Limonioideae, etc. (see Maury 1886). Williams et al. (1994) suggested that it was not known if the mucilage glands were vascularized, although in their data matrix the family was scored as having such glands. Leaf vernation is variable, being flat, convolute or involute.
The style branches of Armeria are papillate all around for their entire lengths. Many Plumbaginoideae seem to lack a protruding obturator (Dahlgren 1916). According to Dahlgren (1916), the embryo sac is tetrasporic but eight-nucleate, but Maheshwari (1947) suggested it was tetrasporic and four-celled, three of the megaspores fused and the mature embryo sac consisted of an egg cell, a single synergid, a tetraploid polar nucleus and a three-nucleate antipodal cell... Aegalitis is little known.
Baker (1948, 1953) discussed variation in floral morphology (pollen, stigmas, etc.), de Laet et al. (1995) discuss floral development, Hegnauer (1969, 1990) chemistry, and there is much general information in Kubitzki (1993b); see Fagerlind (e.g. 1938b) for the development of the embryo sac.
Phylogeny. Lledó et al. (1998, 2001) suggest phylogenetic relationships within the group. For a phylogeny focusing on Limonium, see Lledó et al. (2005). It has also been suggested that Aegialitis may be sister to the rest of the family (Savolainen et al. 2000 - rbcL only); some of the characters attributed to Plumbaginaceae as a whole may need confirmation.
Classification. The classification here is based on the phylogeny in Lledó et al. (1998, 2001). There are a number of monotypic genera in Limonieae (Kubitzki 1993b).
Previous Relationships. Plumbaginaceae used to be associated with Primulaceae. Both have stamens opposite the petals, common petal-stamen primordia, and a ± connate corolla (the latter especially in Limonioideae), but the two are not close - for Primulaceae, see Ericales.
POLYGONACEAE Jussieu, nom. cons. Back to Caryophyllales
Shoots monopodial, branching from previous flush; cork subepidermal (pericyclic); dark-staining deposits, esp. in rays; stem bundles distinct, persistent; pits vestured; nodes also 5 or more:5 or more; petiole with a (D-shaped) ring of bundles, (wing bundles +); mucilage cells common; soluble calcium oxalate accumulation; cuticle waxes as platelets or rodlets; (stomata dia- aniso- or paracytic); lamina vernation revolute, (margins lobed), secondary veins also palmate, colleters +; inflorescences racemose, with flowers in fascicles; flowers small, pedicels articulated; hypanthium ± developed; P +, basally ± connate, usu. some or all members with a single trace; stamens = to and alternate with P to 3 x P; pollen tricolporate to pantoporate; nectary disc-like, or between A (0); G [(2) 3 (4)], (common style short), stigma ± penicillate or capitate; ovule straight, (unitegmic), nucellar beak +, hypostase +, funicle short; (megaspore mother cells several); fruit indehiscent, a trigonous (lenticular) achene; seed ruminate; embryo straight to curved, lateral or not; expansion of the chloroplast inverted repeat.
43[list]/1110 - four groups below. World-wide. [Photos - Collection]
1. Symmerioideae Meisner
Petiole winged, ± surrounding stem, not forming closed tube; plant dioecious; P 6; staminate flowers: A 20+; carpellate flowers: ovary with basal septum; achenes pyramidal, 3 P adnate to wall; n = ?
1/1: Symmeria paniculata N. South America, West Africa (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Tropicos i.2013).
[Afrobrunnichia [Polygonoideae + Eriogonoideae]]: stipule adaxial, tube-shaped, ensheathing stem [= "ochrea"].
Liane climbing by bifid, axillary tendrils; pedicel winged on both sides; P 5; fruit a ?drupe ["turgid"]; seed deeply longitudinally 3-sulcate, irregularly ruminate; n = ?
1/2. Tropical West Africa, Liberia to the Congo (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
[Polygonoideae + Eriogonoideae]: seed not ruminate (ruminate).
(Map: from Hultén 1971; Frankenberg & Klaus 1980; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase i.2013; Australia's Virtual herbarium i.2013; Tanya Schuster, pers. comm.; IndoMalesia incomplete).
3. Polygonoideae Eaton
Herbaceous (annuals), shrubby, lianes or vines [with ?leaf tendrils]; (leaves convolute - Muhlenbeckia), stipule ± scarious; P (3-6); A (3-9); funicle long or short; n = 7 and up.
15/590: Polygonum (200+, if split, then Persicaria 150), Rumex (200), Calligonum (80), Rheum (60). Especially (warm) north temperate.
Synonymy: Calligonaceae Khalkuziew, Persicariaceae Martinov, Rumicaceae Martynov
4. Eriogonoideae Arnott
Lianescent and with branch tendrils [?plesiomorphic], or trees, (herbs); (petiole bundles scattered - some Coccoloba); stipules various, massive, scarious, 0; (plant dioecious); (inflorescence ± cymose, with involucre - Eriogonum et al.); n = ?
28/520: Eriogonum (250, but paraphyletic), Coccoloba (120). Largely tropical, America and the Antilles (West Africa), Eriogonum and relatives esp. W. North America.
Synonymy: Eriogonaceae G. Don
Evolution. Divergence & Distribution. If Oxygonum is sister to [Polygonaceae + Eriogonoideae], it may suggest that Polygonaceae were originally African (Schuster et al. 2011b). Eriogonum and relatives are very diverse in the drier regions of southwest North America (and some apecies also in southern South America), and may represent a relatively recent radiation (Sanchez & Kron 2008).
Diversification within Rheum occurred along with the uplift of the Tibetan Plateau in the last (16.1)-12.0, 9.9(-6.8) m.y.a. (Sun et al. 2012).
Pollination Biology. Remarkable "glasshouse bract" inflorescences with large white recurved inflorescence bracts have evolved twice within Rheum growing at high altitdes in Southeast Asia (Sun et al. 2012). Some species of Rumex have an X-Y system determining the 'sex' of the plant; polyploids may have only a single Y chromosome (Cuñado et al. 2007).
Ecology & Physiology. Calligonum is a clade of C4 plants that is a component of the halophilic vegetation in Asian Turanian deserts, dominated by C4 Chenopodiaceae (Winter 1981; Sage et al. 2011; Christin et al. 2011b for dates). Calligonum can grow to 8 m tall (Winter 1981).
Plant-Animal Interactions. Lycaena and Heliophorus (Lycaenini) are found on Polygonaceae throughout its extratropical range (Ehrlich & Raven 1964), and caterpillars of the lycaenid Euphilotes eat a number of species of Eriogonum (Shields & Reveal 1988).
Bacterial/Fungal Associations. Interestingly, in view of the general paucity of mycorrhizae in Caryophyllales, endomycorrhizae are reported from Eriogonum and ectomycorrhizae from Coccoloba (Malloch et al. 1980) and tundra Polygonum (e.g. Michelsen et al. 1998).
Chemistry, Morphology, etc. Williams et al. (1994) noted that although no plumbagin had been reported from the family, other quinones were known there.
Sieve tube plastids with protein fibres are reported from Triplarieae (Behnke 1999). Woodiness seems to have evolved several times from the herbaceous habir (Lamb Frye & Kron 2003; Tian et al. 2011); it is not a very good indicator of relationships. The climber Antigonon has leaf tendrils and successive cambia (Carlquist 2003a). There are often subepidermal strands of collenchyma or sclerenchyma in the stem in Polygonaceae (see also Plumbaginaceae).
There have been suggestions that the perianth of Polygonaceae are basically 3-merous and two-whorled; the carpels are opposite the outer perianth whorl (e.g. Galle 1977 for floral diagrams, etc.; see also Laubengayer 1937; Ronse Decraene 1989a; Vautier 1949 for floral vascularization). Flowers with five tepals would then be derived from those with six, perhaps by fusion of two of the members. Recent work, however, suggests that the basic condition for the family is to have five perianth members (Lamb Frye & Kron 2003; Burke et al. 2009, 2010; Ronse de Craene & Brockington 2013). However, the extensive earlier work on floral vascularization is not integrated into this scenario, indeed, floral vascularization is unknown for Symmeria, Afrobrunnichia and Oxygonum, phylogenetically critical taxa (see below.
Stamens in Fagopyrum are both introrse and extrorse (Le Maout & Decaisne 1868), while in Persicaria campanulata five stamens are adnate to the perianth and three are completely free (Ronse Decraene & Akeroyd 1988). The exact nature of the funicle is unclear; it might be a reduced basal placenta.
For more information, see Hutchinson and Dalziel (1928: Afrobrunnichia), Vautier (1949: comprehensive survey of floral vasculature), Hegnauer (1969, 1990: chemistry), Ronse Decraene and Smets (1991c: nectaries), Haraldson (1978: general), Brandbyge (1993: general), Ronse Decraene et al. (2000c: fruits in some Polygonoideae), Carlquist (2003a: wood anatomy) and Logacheva et al. (2008: especially expansion of the inverted repeat).
Phylogeny. in the past, the largely herbaceous Eriogonoideae s. str., i.e. Eriogonum and its immediate relatives, were separated from Polygonoideae, variable in habit. The former lacked a sheathing stipule, their inflorescence was cymose and had an involucre, while the latter had a sheathing stipule and a racemose inflorescence that lacked an involucre. However, studies show a different division of the family into two moderately/well supported major clades, largely woody (Eriogonoideae s. l.) and largely herbaceous (Polygonoideae) respectively (Cuénoud et al. 2002; Lamb Frye & Kron 2003; Burke et al. 2010; Sanchez et al. 2011).
Some genera are basal to these two clades. Symmeria and Afrobrunnichia (position of latter not so clear - see above) may be immediately below the [Antigonon + Brunnichia] clade in Eriogonoideae (Sanchez et al. 2009a; Sanchez & Kron 2009; see also Burke et al. 2009). However, Sanchez et al. (2009b) found that Symmeria was sister to the whole of the rest of the family and Afrobrunnichia sister to Eriogonoideae (chloroplast data), Afrobrunnichia was sister to Polygonoideae and Symmeria sister to Eriogonoideae (ITS data), but in a combined analysis the relationships were [Symmeria [Afrobrunnichia [the rest of the family]]]. Not all support values were high, but this set of relationships was found by Schuster et al. (2011b), who also noted that the position of Oxygonum was uncertain, although it, too, might be part of a basal pectination (see also Burke et al. 2010 and Sanchez et al. 2011 for the position of Symmeria).
Eriogonoideae s. l. include the woody Coccolobeae which appear to be both basal and paraphyletic (e.g. Cuénoud et al. 2002; Lamb Frye & Kron 2003); [Antigonon + Brunnichia], both lianes, are sister to the rest of the woody clade (Sanchez & Kron 2008; Burke et al. 2010). Within the rest of Eriogonoideae are clades with 5 and 6 perianth members, although the 5-membered Podopterus may be sister to the 6-membered clade (Burke et al. 2010). Eriogonum is paraphyletic and includes taxa like Chorizanthe and Dedeckera (Sanchez & Kron 2006, 2008); indeed, although tribal limits in the old Eriogonoideae are holding up, subtribes and below are in somewhat of a state of disrepair (Kempton 2012).
The mostly viney Muehlenbeckia is to be included in Polygonoideae; most species are sister to Fallopia (Schuster & Kron 2008; Schuster et al. 2011a). For a molecular phylogeny of Polygoneae, see Schuster et al. (2011b). Rheum shows substantial morphological variation but little molecular variation, at least in the markers analysed (Wang et al. 2005).
Classification. For a tribal classification of Polygonoideae, see Sanchez et al. (2011) and for that of Eriogonoideae (and a subfamilial classification, too), see Burke and Sanchez (2011). Generic limits around Polygonum are difficult, and the tendency now is to split the genus (e.g. Ronse Decraene & Akeroyd 1988; Brandbyge 1993; Ronse De Craene et al. 2004; Kim & Donoghue 2008; Kim et al. 2008; Galasso et al. 2009: comprehensive treatment; Yurtseva et al. 2010).
Thanks. I thank Adriana Sanchez for comments.
[Rhabdodendraceae [Simmondsiaceae [[Asteropeiaceae + Physenaceae] [Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.]]]]: (successive cambia +); styles stigmatic their entire length; ovules 1-2/carpel; fruit 1-seeded; endosperm slight.
Evolution. Divergence & Distribution. This clade may have diverged from the [Droseraceae group [Tamaricaceae group + Polygonaceae group]] clade 82-76 m.y.a., but diversification of the core Caryophyllales did not occur until substantially later at some 47-39 m.y. (Wikström et al. 2001).
Few (1-2) ovules per carpel may be an apomorphy for the whole clade, but the position of these ovules varies - apical in Simmondsiaceae, and basal in Rhabdodendraceae, just for starters. Basifixed anthers and stamens with very short filaments are common outside core members of this clade; their optimisation on the tree is difficult. Taxa with such stamens also lack floral nectaries.
Ecology & Physiology. Robert et al. (2011) note that woody taxa with successive cambia often (86% of cases, lianes/vines not included) grow in conditions in which there is some kind of water stress. They noted that in at least some core Caryophyllales both xylem and phloem are organized to form a three-dimensional network.
Chemistry, Morphology, etc. The morphology, etc., of the basal members of this clade, poorly known though they are, seem rather different from those of the core members.
Phylogeny. Relationships around here are somewhat jumbled in the tree presented by Qiu et al. (2010).
RHABDODENDRACEAE Prance Back to Caryophyllales
Woody; ellagic acid +; cork?; successive cambia + (0); true tracheids +; dark-staining deposits esp. in rays; pits vestured; sieve tube plastids with protein crystalloids and starch; nodes 5- or 7-lacunar; (cortical bundles +); secretory cavities with resin; sclereids +; petiole bundle annular, bundles separate or not, (medullary bundles +), wing bundles +; foliar (branched) fibre-like sclereids +; hairs peltate, cells with SiO2 bodies; lamina punctate, vernation revolute, secondary veins looping close to margin; inflorescence axillary, branched, ?with a terminal flower; hypanthium +, short; K ± connate, short, C rather thick; A many, development ± simultaneous, anthers much longer than filaments, basifixed, wall development monocotyledonous, exodermis tanniniferous; nectary 0; G 1, stylulus basal, stigma much elongated, ?type; ovules 1 (2)/carpel, basal, campylotropous, bitegmic zone short, outer integument 4-5 cells across, inner integument 2-5 cells across, parietal tissue 10+ cells across, nucellar cap 0; megaspore mother cells several; fruit a drupelet, basally surrounded by K/swollen receptacular area, pedicel swollen; exotestal cells tangentially elongated, underlying cells short-tracheidal; perisperm +, slight, endosperm slight, embryo green, with large cotyledons; n = 10.
1[list]/3. Tropical South America (map: see Prance 1972c). [Photo - Flower]
Chemistry, Morphology, etc. I have not seen stipules (see also Puff & Weber 1976; c.f. Prance 1972c), but the rather broad petiole base can be confused with them. The ovule is often described as being unitegmic (e.g. Nandi et al. 1998, following Puff & Weber 1976; but see Tobe & Raven 1989). The styluli may be stigmatic for only part of their lengths. The embryo is surrounded largely by testa that develops from the unitegmic part of the ovule, and the description above refers to this (Tobe & Raven 1989).
For general information, see Prance (2002).
Previous relationships. The position of Rhabdodendraceae has long been uncertain. Thus they were placed in Rutales by Takhtajan (1997), although Prance (1968) had much earlier suggested a position in this general area.
[Simmondsiaceae [[Asteropeiaceae + Physenaceae] [Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.]]]: nodes 1:1; P +, C 0.
Pollination Biology & Seed Dispersal. The absence of petals is tentatively pegged to this node, the implication being that petal-like structures common in members of this clade are in fact staminodial or calycine in origin (Ronse de Craene 2007); see also Brockington et al. (2009), Ronse de Craene and Brockington (2013), and the discussion below under Core Caryophyllales.
SIMMONDSIACEAE van Tieghem Back to Caryophyllales
Evergreen shrubs; ellagic acid 0, seeds with C36-C46 long straight-chain wax ester [jojoba oil - a wax]; successive cambia +; pericyclic fibres +; cork pericyclic; true tracheids +; stomata cyclocytic and laterocytic; hairs uniseriate; leaves opposite, articulated near stem, lamina vernation flat, secondary veins ascending from near base; plant dioecious; flowers small, (4, 6-merous); nectary 0; staminate plant: inflorescence usu. terminal, cymose; A 2x P, extrorse, anthers much longer than filaments, basifixed; pollen ± porate, central part operculoid, spinules minute; carpellate plant: flowers single axillary; G , styles papillate all around; ovule 1/carpel, subapical, pendulous, apotropous, outer integument 6-10 cells across, inner integument 3-5 cells across, parietal tissue to 10 cells across, (nucellar cap to 2 cells across), obturator 0; fruit a capsule, columella persistent, K accrescent, spreading; testa multiplicative, vascularized, exotestal cells palisade, walls thickened, mesotesta aerenchymatous, rest collapsed; endosperm nuclear, reserve?, cotyledons incumbent; germination hypogeal; n = 13.
1[list]/1: Simmondsia chinensis (!: note the epithet). S.W. North America, the Sonoran Desert (map: see Sherbrooke & Haase 1974). [Photos - Collection]
Chemistry, Morphology, etc. The large embryo contains liquid wax made up of esters of high molecular weight, mono-ethylenic acids. The stamens are described as being latrorse (Takhtajan 1997).
For general information, see van Tieghem (1897: cork ?superficial), Mathou (1939) and Köhler (2002), for embryology, see Wiger (1935), for chemistry, see Hegnauer (1989, as Buxaceae), for testa anatomy, etc., see Tobe et al. (1992), and for wood anatomy, see Carlquist (2002b).
Previous Relationships. Simmondsiaceae have usually been included in Buxaceae or placed in a separate family, but close to Buxaceae. However, a monotypic Simmondsiales have been included in Hamamelididae (Takhtajan 1997).
[[Asteropeiaceae + Physenaceae] [Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.]]: ?
[Asteropeiaceae + Physenaceae]: young stem with vascular cylinder; wood parenchyma aliform-confluent; vasicentric tracheids +, fibre tracheids +; rays 1-2 cells wide; A latrorse.
Chemistry, Morphology, etc. Some information on the general anatomy of these two families is taken from Harms (1893); Carlquist (2006) compares their wood anatomy.
ASTEROPEIACEAE Reveal & Hoogland Back to Caryophyllales
Evergreen trees or scrambling shrubs; plant ectomycorrhizal; ellagic acid?; pericyclic fibres +; petiole bundle annular; cortical and mesophyll sclereids +; hypodermis several layered; ?stomata; inflorescence terminal, branched, pedicels with many bracteoles; C +, deciduous; A 9-15, anthers dorsifixed, filaments basally connate; (pollen 6-rugate); G [(2) 3], (style short, stigma lobed), stigma continuous across G; ovules 2-many/carpel, ± apical, ?micropyle, nucellar cap 0; fruit nutlike, (several-seeded), K accrescent, spreading, forming wings, A persistent; seed coat?; endosperm reserve?, embryo curved, cotyledons spirally coiled; n = ?
1[list]/8. Madagascar. [Photos - Collection]
Evolution. Bacterial/Fungal Associations. Asteropeia has both ecto- and arbuscular mycorrhizae (Ducousso et al. 2008; Bâ et al. 2011a, b).
Chemistry, Morphology, etc. Some information is taken from Beauvisage (1920: anatomy), Miller (1975: wood anatomy), Morton et al. (1997b: general), Schatz et al. (1999: revision), and Kubitzki (2002d: general).
Previous Relationships. Asteropeiaceae were previously often included in Theaceae or Theales (Cronquist 1981; Takhtajan 1997), but are very different in wood anatomy (Baretta-Kuipers 1976); the rays are uniseriate.
PHYSENACEAE Takhtajan Back to Caryophyllales
Shrub or tree; triterpene glycosides, oxohexadecanoic acid [keto fatty acid] +; ellagic acid?; pericyclic sclereids +; cuticle wax crystalloids?; ?petiole bundle; leaves two-ranked; plant dioecious; inflorescence axillary, racemose, pedicels long; P 5-9; staminate flowers: A (8-)10-14(-25), anthers much longer than filaments, long, basifixed; carpellate flowers: G , septae incomplete, 2 ± subbasal campylotropous ovules/carpel, funicle long; fruit subdrupaceous?; seed large, coat vascularized, 16-20 layers thick, cell walls not notably thickened; endosperm 0, reserve?, cotyledons unequal; n = ?
1[list]/2. Madagascar. [Photos - Collection]
Chemistry, Morphology, etc. The petiole is often described as being articulated; it commonly breaks transversely above the base, but there is no evidence that the leaf is derived from a compound leaf. The vascular bundles in the lamina are completely surrounded by mechanical tissue. There are brachysclereids in the secondary phloem and the placental bundles are inverted (Dickison & Miller 1993).
General information is taken from Morton et al. (1997b) and Dickison (2002); for triterpene glycosides, see Inoue et al. (2009).
Previous Relationships. Physenaceae were included in Urticales by Cronquist (1981) and placed in a monotypic Physenales in Dilleniidae by Takhtajan (1997).
[Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.] / Core Caryophyllales: plant herbaceous; (CAM [especially pervasive in succulents] and C4 photosynthesis common); ferulic acid ester-linked to primary unlignified cell walls; (O-methylated) flavonols, quinones, triterpenoid saponins +, tannins, myricetin 0 or slight; (phytoferritin +); sieve tube plastids with a ring of proteinaceous filaments and a central angular crystalloid (also with starch); pericyclic fibres 0 [phloem-derived fibres quite widespread]; (mucilage cells +); (stomatal orientation transverse); inflorescence cymose; (stamens equal and opposite perianth members); pollen trinucleate, (polyaperturate), foot layer thin; nectaries on adaxial bases of stamens [or hypanthium]; G with median member adaxial, stigmas papillate, little expanded; ovules campylotropous, (space between the bases of the inner and outer integuments), (placental obturator +, papillate), (funicles long); fruits with more than one seed, seeds black; both exotestal and endotegmic cells thickened, (space between testa and tegmen), bar-like thickenings on endotegmic cells; endosperm 0, perisperm +, starchy, starch grains clustered, embryo curved, not central, cotyledons incumbent; introns lost in mitochondrial rps 10 and chloroplast rpl2 [latter present in some Portulaca?] genes.
Evolution. Divergence & Distribution. Core Caryophyllales contain ca 5.3% of eudicot diversity (Magallón et al. 1999). Fossils identified as Amaranthaceae have been dated to the Santonian/Campanian of ca 83 m.y.a. (Magallón et al. 1999), but molecular estimates of its age are only some 28-40 m.y. (Wikström et al. 2001) - something is clearly wrong.
The evolution of petals, betalains and anomalous secondary thickening in this group has long been of interest, but relationships along the spine of the tree and the sampling of taxa for betalains and secondary thickening in particular need to be improved to understand better what is going on. However, it seems unlikely that the presence of betalains is plesiomorphic (Brockington et al. 2011; c.f. Cuénoud et al. 2002; Cuénoud 2002a; see also Clement & Mabry 1996); the evolution of normal secondary thickening is unclear. Both anthocyanin and betalain synthesis may have been acquired, lost, or flipped from one to the other more than once, the exact pattern of gains/losses/transitions depending on the optimisation procedure followed (Brockington et al. 2011).
The evolution of corolla-like structures is not simple (see Ronse de Craene 2010 for numerous floral diagrams of this group). Any "corolla" present, as in Caryophyllaceae, is usually described as being of staminal origin (e.g. Ronse Decraene & Smets 1993; Leins et al. 2001), although as Greenberg and Donoghue (2011) noted, it was perhaps surprising that petals in Caryophyllaceae are found in a clade in which stamen number has increased from 5 to 10; Caryophyllaceae with 5 stamens only rarely have petals. In taxa with a single perianth whorl, perhaps equivalent to the "calyx" of Caryophyllaceae, this whorl quite often becomes attractive and corolline, bracteoles then often being calycine. "Petals" may have evolved maybe nine times or so in the clade and in a variety of ways (Brockington et al. 2009; see also Ronse de Craene & Brockington 2013). Brockington et al. (2012) showed that not only are the "petals" of Aizoaceae-Ruschioideae and -Mesembryanthemoideae of probable staminal origin, but also B-class genes are not involved in their development.
The evolution of ovule number is also very labile. Thus a single ovule/ovary could be a synapomorphy for all Core Caryophyllales minus Macarthuria, but two or more ovules/ovary would have evolved more than once, and the single ovule/carpel condition regained - and a distinction may have to be made between a single ovule/carpel and a single ovule/ovary. In fact, the whole clade (Rhabdodendraceae on up) may be characterizable by its low ovule number.
Ecology & Physiology. Taxa growing in saline and/or dry conditions are noticeably well represented here, and taxa that can grow on gypsum (hydrous calcium sulphate) are scattered throughout the clade (Douglas & Manos 2007). Such habitats are not ideal for mycorrhizal fungi, and they are not often reported from Caryophyllales at all (but see Newman & Reddell 1987). Succulents are common, and many taxa have C4 photosynthesis, CAM or their variants (Ehleringer et al. 1997; Sage et al. 2012; see also Ocampo & Colombus 2010; Christin et al. 2011b for dates). C4 photosynthesis is most common here outside Poales, indeed, about one half (33/62) of all evolutionary origins of the syndrome in angiosperms occur in core Caryophyllales (Sage et al. 2011).
Plant-Animal Interactions. Core Caryophyllales are little liked by butterfly caterpillars (Ehrlich & Raven 1964).
Bacterial/Fungal Associations. A white blister rust, Wilsoniana, an oomycete, is found parasitic on taxa scattered throughout this clade (Thines & Voglmayr 2009 and references).
Chemistry, Morphology, etc. Details of betalain synthesis are poorly known, although tyrosine is the starting point; after modification, it forms the chromophore for both betalain and betaxanthins, yellow pigments (Tanaka et al. 2008; Pichersky & Lewinsohn 2011). The differences between betalain and anthocyanin synthesis pathways may not be that great (Strack et al. 2003; Shimada et al. 2007), while Shimada et al. (2005) found that anthocyanidin synthase genes were expressed in the seeds of both Phytolacca and Spinacia. For tannin (both classes) distribution, see Mole (1993). Sterol composition may be of systematic interest (Wolfe et al. 1989; Patterson & Xu 1990), with distinctive sterols common or dominant in Caryophyllaceae, Phytolaccaceae, Amaranthaceae, and "Portulacaceae". Isoflavonoids (Reynaud et al. 2005), sometimes quite diverse, and phytoecdysones are scattered in the Core Caryophyllales, but perhaps not in the Cactaceae area.
Stomatal morphology is variable, but anomocytic stomata are common in nearly all families. However, in Cactaceae and relatives, parallelocytic and other kinds of stomata are found; some families in this area have predominantly paracytic stomata. Stomatal orientation on stem and/or leaf is commonly transverse apparently throughout the order (Butterfass 1987, ?Amaranthaceae s. str.?), however, it is unlear which taxa have vertically or which unoriented stomata. Variation in structures associated with the leaf base, whether hairs or "stipules", is considerable (Rutishauser 1981) and would repay further study; note that the basic nodal anatomy of the clade is one trace-one gap, unusual for plants with stipules as commonly accepted.
For a good general survey of floral morphology, see Hofmann (1994). Sepals with an abaxial crest are described from Caryophyllaceae, Amaranthaceae, Aizoaceae, and Portulacaceae (Ronse de Craene & Brockington 2013). If there is a "corolla", it arises at the same time or after the androecium, not before it, and the "petals" and stamen(s) opposite them may form a developmental unit (e.g. Eichler 1875; Wagner & Harris 2000). The corona - in Lychnis viscaria, at least - arises from two bulges on the adaxial side of the "corolla", perhaps representing anther thecae.
When the stamens are equal in number to the perianth members they are opposite to them, when there are many stamens the initial primordia either alternate with them (Aizoaceae), or continue the spiral of the tepals (Pereskia - Cactaceae: see Leins & Erbar 1994a, b); development is centrifugal.
The carpels are quite commonly open in development - also in Polygonaceae (Tucker & Kantz 2001). Placentation is quite variable, although one commonly thinks of this group as having free-central placentation or its variants. A subepidermal layer of cells in the inside of the ovary wall may have calcium oxalate sand, as in some Amaranthaceae and Polygonaceae(!), while in Nyctaginaceae a ring of cells immediately below the ovary have conspicuous raphides (Guéguen 1901); there is little information on this feature. The apical cells of the nucellus are commonly elongated radially, as in Cactaceae, "Portulacaceae", Aizoaceae, Phytolaccaceae, and Amaranthaceae (see Johri et al. 1992), i.e., they form a nucellar pad, but it is unclear if this feature is of systematic significance. Narayana (1962: e.g. Aizoaceae, Gisekiaceae, Molluginaceae) showed cells over the apex of the embryo sac as being in radial files, i.e., they seem to form a nucellar cap, as is found in e.g. Phytolaccaceae and Chenopodiaceae. The integuments are often separated by a small space at their bases, but this seems to vary within Portulaceaeand Cayophyllaceae, and be absent in Phytolacca and Amaranthaceae (e.g. Meunier 1890; Hakki 1973; c.f. Bittrich 1993). The cells of the parietal tissue in radial rows in some families, but whether they are or not seems to vary within Portulaca and Mesembryanthemum (Meunier 1980). There are often short hairs on the funicle that are directed towards the micropyle (Neumann 1935).
Seeds of a number of taxa have an operculum, although not necessarily identical in morphology (Bittrich & Ihlenfeldt 1984). There are commonly bar-like thickenings on the walls of the endotegmic cells (e.g. Netolitsky 1926; Bittrich 1993a; perhaps shown in Narayana 1962a), although these are absent from most Caryophyllaceae, at least - a complete survey would be useful. Zheng et al. (2010) note that the starchy perisperm tissue is formed not from the parietal tissue surrounding the embryo sac, but from tissue immediately below the embryo sac, i.e., it is technically chalazosperm. For the loss of the intron of the rpl2 gene, see Logacheva et al. (2008).
Additional information is taken from Bittrich (1993a: useful general summary), Hegnauer (1989: general chemistry), Wolfe et al. (1989: sterols), Patterson & Zu (1990: sterols), Steglich and Strack (1990: betalains), Strack et al. (2003: betlains), Shimida et al. (2007: control of anthocyanin/betalain production), Barthlott (1994: waxes), Behnke et al. (1983a: sieve tube plastids), Behnke (1994a: sieve tube plastids, phytoferritin), Gibson (1994), Jansen et al. (2000c) and Ostroumova and Timonin (2011), anatomy, esp. successive cambia, Meunier (1890: ovules and testa), Zandonella (1977: nectaries), Rutishauser (1981: "stipules" and similar structures), Nowicke (1994: pollen), Werker (1997: seed coat), Cuénoud (2006: summary) and Sage et al. (1999) and Muhaidat et al. (2007 and references) for the C4 pathway.
Phylogeny. [Amaranthaceae [Achatocarpaceae + Caryophyllaceae]] were early found to form a moderately well supported clade, the rest of the core Caryophyllales another (Källersjö et al. 1998), however, although 13 families were included in this study, sampling within them was poor. Similar relationships were suggested by Savolainen et al. (2000a). D. Soltis et al. (2000) found that Phytolaccaceae, Nyctaginaceae and Delosperma (Aizoaceae) formed a group, also [Amaranthaceae + Caryophyllaceae], but again the sampling was very sparse; for the position of Achatocarpaceae, see also Müller and Borsch (2005). For other ideas of relationships, see Rodman (1994) and Downie and Palmer (1994: structural variation in chloroplast DNA).
Many of the relationships in the tree here are like those suggested by Cuénoud et al. (2002: the Delosperma sequence was excluded, sampling still a bit sketchy), and these are largely similar to relationships found by Källersjö et al. (1998) and other workers. Cuénoud et al. (2002) found two quite well supported clades within core Caryophyllales. Aizoaceae were monophyletic, albeit with only slightly better than marginal (52% bootstrap) support in an analysis of matK sequences, the only gene for which they had moderately good sampling; Gisekia moved position in analyses of rbcL and matK sequences; and Sarcobatus was sister to Nyctaginaceae, albeit with only weak support, in matK analyses, while in a rbcL analysis it grouped with Agdestis (Cuénoud et al. 2002). Relationships around Cactaceae, themselves a monophyletic group, remained difficult, and although progress has recently been made here (Brockington et al. 2009; Nyffeler & Eggli 2009; Ocampo & Columbus 2010; Soltis et al. 2011: see also below), some relationships still remain uncertain. However, Arakaki et al. (2011: see below) have produced a largely resolved tree of that area. Harbaugh et al. (2010) found that Molluginaceae were sister to Caryophyllaceae, rather than Amaranthaceae, although two taxa from both families were all that were included in their study, which focused on Caryophyllaceae. Stegnospermataceae were sister to all other core Caryophyllales (support quite strong) and Limeum was placed with Amaranthaceae (support also quite strong) in a mitochondrial analysis by Qiu et al. (2010); however, Caryophyllaceae were not included. Support for the grouping [Stegnospermataceae [Caryophyllaceae + Amaranthaceae]] was found by Moore et al. (2011). Crawley and Hilu (2012) examined the effect of missing data and missing taxa on phylogenetic reconstructions here.
There have been recent major improvements in our understanding of relationships along the backbone of core Caryophyllales. Schäferhoff et al. (2009) found that the poorly-known Microtea, one of whose previous resting places was Phytolaccaceae, was sister to the rest of core Caryophyllales, but in a more recent study, Macarthuria, previously included in Limeaceae (and before that in Molluginaceae), occupied that position, and with strong support (Christin et al. 2011a: Microtea not included); Limeum, with which Macarthuria was previously associated, remained in its old position well embedded in core Caryophyllales. Furthermore, Corbichonia (Lophiocarpaceae) and most of Hypertelis (one species was previously in Molluginaceae) were well supported as successive sister clades at the base of the [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]] clade (Christin et al. 2011a); Hypertelis was also found to be in this general area of the tree in Schäferhoff et al. (2009: they included it only in their petD analysis). Here both Macarthuria and Hypertelis are placed separately on the tree (see also Brockington et al. 2011), although it is not clear exactly what the support values for these positions are. Arakaki et al. (2011) found that Gisekiaceae and Aizoaceae reversed positions, but with little support, but this area was not the focus of their study.
So progress is definitely being made. However, detailed sampling of Phytolaccaceae as well as Molluginaceae is essential if we are to understand relationships and evolution within core Caryophyllales. Even if only some of the new placements just mentioned are confirmed - and confirmation is badly needed - character evolution may well have to be reorganized. Before character reconstruction is attempted, ensuring that basic phytochemical, morphological and anatomical studies on the migratory taxa just mentioned is very much needed. In general, morphological distinctions between those clades that can be recognised are slight.
Previous Relationships. Most of this group was included in the old Centrospermae (so named because of the basal or free-central placentation that is common in the clade) or Caryophyllales in the strict sense. The shikimic acid pathway, particularly phenylalanine, is a starting point for the synthesis of nitrogen-containing benzylisoquinoline alkaloids and the betalains of core Caryophyllales, and Kubitzki (1994) suggested a relationship between core Caryophyllales, Magnoliidae and monocots because all contained such compounds.
MACARTHURIA Back to Caryophyllales
±Rigid, rush-like shrubs; O-glycosylflavonoids, anthocyanins +; cork?; secondary growth abnormal; sieve tube plastids also with starch grains; nodes?; leaves spiral, at least some reduced to scales; K 5, C 0, 5, adnate to base of staminal tube; A 8, connate basally; G [3(-7)]; ovules 1-3/carpel, embryology?; fruit a leathery capsule; seeds with funicular aril; n = ?
1/10. Australia, the periphery, esp. S.W. Australia (map: from Lepschi 1996; FloraBase vi.2011).
Evolution. Pollination Biology & Seed Dispersal. The seeds of Macarthuria are myrmecochorous (Lengyel et al. 2010).
Chemistry, Morphology, etc. The genus is poorly known. For further information, see Hofmann (1973: flower, growth), Behnke et al. (1983b: pollen, sieve tube plastids, etc.), M. Endress and Bittrich (1993: general, as Molluginaceae), Lepschi (1996: general), and Hassan et al. (2005a: seed coat).
Previous Relationships. In earlier versions of this site (pre vi.2011) Macarthuria was included in Limeaceae; M. Endress and Bittrich (1993) placed it in Molluginaceae.
[Microteaceae [[Caryophyllaceae [Achatocarpaceae + Amaranthaceae]] [Stegnospermataceae [Limeaceae [[Lophiocarpaceae [Hypertelis [Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]]]]: betalains [chromoalkaloids]; placentation free-central or basal.
Evolution. Divergence & Distribution. It is unclear whether the acquisition of betalains is to be placed at this or a deeper node (see also Brockington et al. 2011).
MICROTEACEAE Schäferhoff & Borsch Back to Caryophyllales
Annual herbs; betalains?; cork?; secondary growth?; sieve tube plastids lacking protein crystalloid, with a central starch grain; nodes?; calcium oxalate crystals 0; leaves spiral; inflorescence racemose, flowers in groups of up to 3; P (4) 5; A (2-)5-9, anthers globose; pollen pantoporate; G [2-4], orientation variable, unilocular, styluli diverging; ovule single [per flower], embryology, funicle quite long; fruit a muricate to spiny achene; seed coat?; n = ?
1/9. Central and South America, Antilles (Map: from TROPICOS, vi.2011).
Chemistry, Morphology, etc. Microtea is very poorly known. Some information is taken from Nowicke (1969: as Phytolaccaceae), Rohwer (1993; as Phytolaccaceae); for sieve tube plastids, see Behnke (1993).
Phylogeny. See Schäferhoff et al. (2009).
Previous Relationships. In Amaranthaceae (early versions of this site), as Phytolaccaceae-Microteoideae Nowicke, sometimes with Lophiocarpus in Phytolaccaceae (Rohwer 1993) or separate Lophiocarpaceae Doweld & Reveal...
[[Caryophyllaceae [Achatocarpaceae + Amaranthaceae]] [Stegnospermataceae [Limeaceae [[Lophiocarpaceae [Hypertelis [Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]]: ?
[Caryophyllaceae [Achatocarpaceae + Amaranthaceae]]: (phytoecdysteroids +); stamens = and opposite P; ovule single [per flower], parietal tissue ca 4 cells across, nucellar cap 2-4 cells across; esp. outer wall of exotesta thickened and with stalactite-like projections; mitochondrial rps1 and 19 genes lost.
Chemistry, Morphology, etc. Achatocarpaceae are poorly known, and most of the characters mentioned above need to be confirmed.
For phytoecdysteroids, see Báthori et al. (1987), Dinan et al. (1998), and Zibareva et al. (2003). Mickesell (1990) listed both Amaranthaceae and Caryophyllaceae as having endosperm haustoria. Sukhorukov (2007) described the exotegmic cells of Chenopodiaceae s. str. as often having tannin deposits in the outer walls of the exotegmic cells that projected into the cell lumen (see also Kadereit et al. 2010).
CARYOPHYLLACEAE Jussieu, nom. cons. Back to Caryophyllales
Herbs (shrubs, lianes); cyclopeptides, anthocyanins, glycoflavones, anthraquinones +; cork usu. pericyclic; true tracheids, fibres +; pericyclic fibres +; nodes often swollen; stomata often diacytic; (cuticle waxes as rodlets); lamina vernation conduplicate or ± flat, stipules +, ± scarious; (plant dioecious); flowers 4-5-merous; hypanthium +; A-C primordium + [how common/]; A (1-4), outer secondary parietal cell dividing, tapetal cells 2-nucleate; (pollen 6(+) porate); (nectary surrounding or abaxial to [esp. antesepalous] A on receptacle); G [2-5], both alternate with opposite "C", when 3 odd member adaxial, placentation axile, styles impressed [distribution?]; ovules lacking parietal tissue, nucellar cap +, (nucellar epidermis dividing along sides of ovules; parietal tissue 3-10 cells across, in radial rows or not), funicle?; fruit an utricle/achene/nutlet; (endotesta thickened; endotegmen ± thickened); embryogeny solanad, initially distinct air space between the cotyledons [?all taxa]; n = 7-15, 17; protein bodies in nuclei; mitochondrial coxII.i3 intron 0; sporophytic self-incompatibility system present.
86[list]/2200 - 11 groups below. Mostly temperate, esp. Eurasian (map: from Vester 1940; Frankenberg & Klaus 1980; Hultén 1971; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase i.2013; Australia's Virtual Herbarium i.2013). [Photos - Collection, Minuartia Habit, Microphyes Flower.]
1. Corrigioleae Dumortier
[Stipules auriculate]; leaves spiral; K with scarious margins; G with incomplete septae; fruit utricle or nutlet; endotegmic cells lacking bar-like thickenings.
2/16. Mediterranean to Pakistan, Africa, Chile; Corrigiola litoralis widely distributed.
Synonymy: Corrigiolaceae Dumortier, Telephiaceae Martynov
[Paronychieae [Polycarpeae [Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]]]]: leaves opposite.
2. Paronychieae Dumortier
[Stipules paired, subadaxial to petiole; paired, connate, adaxial; single, concave, adaxial or interpetiolar]; P hooded, with subapical abaxial awn, (with scarious margins), (C +, filiform); (staminodes +); fruit a nutlet.
15/190: Paronychia (110), Herniaria (45). Worldwide, esp. Paronychia, many genera Mediterranean to Middle Eastern.
Synonymy: Herniariaceae Martynov, Illecebraceae R. Brown, nom. cons., Paronychiaceae Jussieu
[Polycarpeae [Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]]]: C +.
3. Polycarpaeae de Candolle
Stipules + [interpetiolar fimbriae, from common primordium]; K usu. hooded, awned, (with scarious margins), (C +, deeply lobed to entire); styles basally connate; (fruit a capsule, seeds ³2/fruit).
Polycarpaea (50), Drymaria (48). Almost worldwide.
Synonymy: Ortegaceae Martynov, Polycarpaeaceae Schur
[Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]] / Plurcaryophyllaceae [sic]: wood rayless [?here]; hypanthium 0; A 10(+); (placentation axile at least basally when ovary young); fruit a septicidal and loculicidal capsule, ³2 seeds/fruit.
4. Sperguleae Dumortier
[Stipules single, interpetiolar, connate and encircling stem below leaves]; K with scarious margin.
Spergula (60). ± worldwide.
Synonymy: Spergulaceae Bartling
[[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]: stipules 0.
[Sclerantheae + Sagineae]: ?
5. Sclerantheae de Candolle
Hypanthium +/0; (K with membranous margins); (C 0); (nectary); A 1-10, (5 staminodes); (fruit a nut, 1-seeded).
Schiedea (34). Northern Hemisphere, Australasia, Ethiopia.
Synonymy: Scleranthaceae Berchtold & J. S. Presl
6. Sagineae Tanf.
Hypanthium +/0; (K awned; with scarious margins); (A = C); (fruit a nut, 1-seeded).
Minuartia (175). Northern hemisphere, tropical montane, temperate southern hemisphere.
Synonmy: Minuartiaceae Martinov, Saginaceae Berchtold & Presl
[[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]: hypanthium 0; capsule often with 2X teeth as styles; embryogeny caryophyllad.
[[Arenarieae + Alsineae]]: ?
7. Arenarieae Kitt.
(Oily funicular aril - Moehringia); cotyledons incumbent.
Arenaria (135). Northern hemisphere, Central and west South America.
Synonymy: Sabulinaceae Döll [?here], Sarcocaceae Adanson [?status]
8. Alsineae Lamarck & de Candolle
(Hypanthium +); (K with scarious margins), C ± retuse; (fruit a nut, 1-seeded).
Stellaria (175), Cerastium (100), Odontostemma (38). Northern Hemisphere, esp. Eurasian, some cosmopolitan.
Synonymy: Alsinaceae Bartling, nom. cons., Cerastiaceae Vest, Stellariaceae Berchtold & J. Presl
[Sileneae [Caryophylleae + Eremogeneae]]: veins at apex of lamina intramarginal; K ± connate; (anthophore [prolongation between K and the rest of the flower] +); C clawed, contorted, apex retuse or not, venation closed, coronal scale +/0.
9. Sileneae de Candolle
K with commissural veins, C variously contorted (imbricate); (placentation axile basally).
?6/738: Silene (700). North Temperate, African montane.
Synonymy: Lychnidaceae Döll, Ortegaceae Martynov, Silenaceae Bartling
[Caryophylleae + Eremogeneae]: ?
10. Caryophylleae Lamarck & de Candolle
("Epicalyx" +); K without commissural veins; C dextrose-contorted (imbricate); G 2 (3); n = 12-15, 16.
17/610: Dianthus (300), Gypsophila (150), Acanthophyllum (75). Eurasia (Africa, Gypsophila australis Australia and New Zealand).
Synonymy: Dianthaceae Vest
11. Eremogoneae Rabeler & W. L. Wagner
Leaves linear, ± rosette-forming; hypanthium poorly (well) developed; K not connate, with scarious margins, hardened at base; cotyledons accumbent.
2/68: Eremegonum (66). (Eur)Asian, west North America.
Evolution. Divergence & Distribution. The earliest fossils associated with Caryophyllaceae seem to be of the pollen Periporopollenites polyoratus, from the Late Campanian ca 73 m.y.a.. This has been linked with the macrofossil Caryophylliflora paleogenica from the Eocene of Tasmania, but these fossils cannot be placed with any known member of the family (Jordan & McPhail 2003).
The diversification rate in European Dianthus is suprisingly high, 2.2-7.6 species/m.y. and (at the time) the highest rate recorded for either plants or terrestrial vertebrates (Valente et al. 2010a). The genus is summer-flowering (i.e. it flowers during the dry season) and contains many narrow endemics (Valente et al. 2010a). Relatives of Schiedia, which forms a substantial radiation on Hawaii, appear to include Honckenya and co., from the Arctic and subarctic (Harbaugh et al. 2009a).
For optimisation of characters, see Greenberg and Donoghue (2011, but c.f. Fig. 5c) in the context of a well-sampled phylogeny.
Pollination Biology & Seed Dispersal. For the evolution of dioecy in Silene, which happened three times or so, see Desfeux et al. (1996) and Zluvova et al. (2008). Species of Silene subgenus Elisanthe have an X-Y 'sex' determination system (Lebel-Hardenack et al. 2002; Charlesworth 2008 and references). Silene and its relatives may be pollinated by moths which at the same time lay eggs on the ovary, rather like the yucca-yucca moth association (Kephart et al. 2006 for literature, see also other papers in that issue of the New Phytologist [169(4)]).
Bacterial/Fungal Associations. Ectomycorrhizae have been reported from the family (Wang & Qiu 2006). For anther smut fungi, see Ngugi and Scherm (2006). Microbotryum violaceum s.l. (Uredinomycota - see also Montiaceae) is common on the family, especially on perennial Sileneae (ca 80% of the species), but not much on the annuals nor on members of the old Paronychioideae; strict cospeciation is not involved (Refrégier et al. 2008; Mena-Ali et al. 2009; Hood et al. 2010).
Genes & Genomes. There has been a massive increase in the rate of synonymous substitutions in the mitochondrial genome of Silene noctiflora, but not in that of the chloroplast genome, nor in the substitution rates of its immediate relatives (Mower et al. 2007). The mitochondrial genome of its relative, S. conica, is at 11.9 mb bigger than the whole nuclear genome of some eukaryotes, while S. latfolia has quite a small mitochondrial genome of only 0.25 mb. Species of Silene with such huge mitochondrial genomes may have over a hundred chromosomes, as least from the evidence of the circular mapping procedures used (Sloan et al. 2012).
Chemistry, Morphology, etc. Variation in stipule morphology in Caryophyllaceae is considerable, even during the course of development of a single plant, as in Paronychia argentea (Rutishauser 1981).
In Pseudostellaria, at least, the stamens are initiated before the corolla (Luo et al. 2012). The long, curved nectary in some species of Schiedia develops on the abaxial bases of the stamens opposite to the calyx (Wagner & Harris 2000; esp. Harris et al. 2012). Weberling (1989 and references, esp. Thompson 1942) discusses placentation, which varies from axile, as in some species of Silene, perhaps the common condition in the family, to free central to the single, basal ovule of Uebelinia (this latter looks rather like a circinotropous basal ovule). Members of the old Paronychioideae have solanad rather than caryophyllad embryo development.
Some general information is taken from Bittrich (1993b); for information on the old Alsinoideae - and a number of maps - see McNeill (1962), for ovules and seeds, see Meunier (1890), for floral morphology, etc., see Rohweder (1967b, 1970a), Rohweder and Urmi-König (1975) and Rohweder and Urmi (1978), for stomata, see Rohweder et al. (1971: correlation between stomatal apparatus and leaf width), for stem anatomy, see Schweingruber (2007), general chemistry, see Hegnauer (1964, 1989), for floral morphology, see Thompson (1942), for stamens or nectaries as corolla, see Mattfeld (1938) and Leins et al. (2001), for the distribution of phytoecdyosteroids, see Zibareva et al. (2003), and of cyclopeptides, see Jia et al. (2004).
Phylogeny. Of the old subfamilies, Paronychioideae - classically defined by the presence of stipules, lack of a corolla, and utricular fruit - form a basal grade, with Corrigioleae (Telephium, Corrigola) sister to the rest of the family. Dicheranthus, Polycarpon, etc., may form the next clade, Paronychia, etc., the next. Drymaria and Pycnophyllum, both morphologically distinctive taxa, may be sister (Smissen et al. 2002 - they noted that Pycnophyllum [and Pentastemonodiscus] were not to be included in Caryophyllaceae-Alsinoideae, but they did not suggest where they should go; Fior et al. 2006). In the erstwhile Alsinoideae the calyx is free and the corolla has ± open venation. Alsinoideae for the most part break down into two groups: one, including Cerastium, Stellaria, etc., has capsules with split valves, and the other including Minuartia, etc., is very diverse, but has capsules with entire valves; the corolla is often bilobed. For Moehringia, the evolution of its strophiole, and its allies, see Fior and Karis (2007 and references). Finally, Caryophylloideae, with their connate calyx and a clawed corolla with more or less closed venation and adaxial appendages (ligules), are holding up better phylogenetically. The tribes Sileneae and Caryophylleae are perhaps monophyletic, and together are sister to or form a polytomy with part of Arenaria (Nepokroeff et al. 2002; Fior et al. 2006).
Harbaugh et al. (2010) have clarified the picture. Relationships - on the whole well supported - from a three-gene analysis are [Corrigolieae [Paronychieae [Polycarpeae [Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]]]]]. Greenberg and Donoghue (2011) sampled more extensively but found a largely similar topology; a group [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae]] did not have much support. The position of the newly described Eremegoneae is uncertain in Harbaugh et al. (2010), but support was stronger in Greenberg and Donoghue (2011); in its current position either it should have as additional apomorphies the apomorphies of the whole [Sileneae [Caryophylleae + Eremogeneae]] clade, but as losses, or these features should arise independently in Sileneae and Caryophylleae... Within Sagineae, Drypis, previously in Caryophylloideae because its connate calyx, etc., is in the same immediate clade as Habrosia (ex Alsinoideae), so the variation there is considerable (Harbaugh et al. 2010; see also Greenberg & Donoghue 2011). The phylogenetic structure now evident in the family has considerable implications for character evolution - see Greenberg and Donoghue (2011) in particular.
For the phylogeny of Dianthus in Eurasia, see Valente et al. (2010a), for Silene and its relatives, perhaps not monophyletic, see Desfeux and Lejeune (1996) and Erixon and Oxelman (2008), and for Viscaria, etc., Frajman et al. (2009).
Classification. The old tripartite division of the family into Silenoideae, Alsinoideae and Paronychioideae based on presence of a hypanthium, whether or not the petals were emarginate, whether the calyx was fused or not, etc., is not confirmed by recent work. Here I follow the tribal classification of Harbaugh et al. (2010, see also 2012: ?Drypidae Fenzl?). These authors did not sample a number of genera, so tribal compositions were uncertain, but the situation was considerably improved by Greenberg and Donoghue (2011).
Features like number of styles and whether there is obviously a common stylar region often provided generic characters in the past. However, the limits of Silene, historically characterised by having three styles, need to be expanded to include some taxa with five styles (Desfeux & Lejeune 1996). Genera like Arenaria and Minuartia are polphyletic (Harbaugh et al. 2009); indeed, many generic limits need attention (Greenberg & Donoghue 2011).
Botanical Trivia. There are reports of placental tissue from 30,000 year old material of Silene stenophylla (or perhaps another species of the genus) trapped in permaforst being persuaded to form whole plants (Yashina et al. 2012a, b).
[Achatocarpaceae + Amaranthaceae]: pollen porate; ovule single, basal.
ACHATOCARPACEAE Heimerl, nom. cons. Back to Caryophyllales
Woody; C-glycosylflavonoids +, betalains?; cork?; secondary growth normal; nodes ?; cuticle waxes as ± lobed platelets in clusters; P 4-5; A 10-20, basally connate or not; pollen 6-porate; G , collateral or superposed; ovules (2), details?; fruit a 1-seeded berry; seeds with small aril; n = ?
3[list]/7. S.W. USA to South America (map: from Fl. N. Am. 4: 2003; GBIF 2008). [Photo © C.E. Hughes - Fruits, Fruiting branch.]
Chemistry, Morphology, etc. Some information is taken from Bittrich (1993b).
AMARANTHACEAE Jussieu, nom. cons. Back to Caryophyllales
Succulent, herbaceous or shrubby (lianes), often in saline conditions; betalaines, anthraquinones, (isoquiniline alkaloids), 6-7-methylene-dioxyflavonols, isoflavonoids +, soluble oxalate accumulation; successive cambia +, inc. roots; wood storied, rayless, esp. when young; vessels in multiples; often a few pericyclic fibres +; cork pericyclic [esp. chenopods; and elsewhere]crystal sand + [less common in chenopods], soluble calcium oxalate accumulation; cortical and/or medullary bundles + [less common in amaranths s. str.]; sieve tube plastids lacking protein crystalloid (starch grain +); nodes often swollen, (1:3, 1:5); petiole bundles ± annular; stomata also paracytic (dia- and anisocytic); hairs variable, often uniseriate, (adaxial to the leaf base - Anabasis); (leaves opposite), lamina margins often toothed; (bracts and bracteoles scarious); P (1-)5(-8), ± herbaceous [chenopods] to scarious; stamens joining nectariferous disc, ± connate or not, (with appendages [pseudostaminodes]), (coloured vesicular anther appendages - Caroxyloneae), anther wall development monocotyledonous, (tapetum plasmodial); pollen multiporate, often starchy, foot layer well developed; G [1-3(-6)], (subinferior), (median member abaxial), placentation basal, (apical), style ± developed, stigmas capitate; ovule also amphitropous, etc., with parietal tissue 3-9 cells across, in radial rows or not, (chalazal region ± digested by the embryo sac); antipodal cells persist, embryo sac haustorium +; fruit surrrounded by a persistent (subfleshy) perianth [anthocarp], bracts and bracteoles persistent and also often part of disseminule, indehiscent, or circumscissile capsule, (berry; drupe); endotegmen ± thickened and lignified, tanniniferous; (perisperm 0), embryo green or white (spiral - Salicornia etc.; straight); n = (6-)8, 9(-17).
174[list]/2050-2500: Chenopodium (100), Atriplex (300), Gomphrena (120), Salsola (100), Alternanthera (100), Iresine (80), Amaranthus (60), Celosia (45), Iresine (45). ± World-wide, esp. warm and dry temperate and subtropics and saline habitats (map: from Hultén & Fries 1986; Jalas et al. 1999; Culham 2007). [Photo - flowers, fruits, Collection.]
Small shrubs; flowers axillary; A 5 (3, 2), (pseudostaminodes +); (anthers unilocular); pollen smooth, (with microspines - Surreya); G ; n = 9.
4/11(-13). Widely scattered, but not tropical or Sahara and southwards.
Synonymy: Sabulinaceae Döll [?here], Sarcocaceae Adanson [?status]
Evolution. Divergence & Distribution. Kadereit et al. (2012) estimate stem Amaranthaceae at 87-47 m.y.a. It is estimated that Polycnemoideae separated from the rest (68.0-)48.6(-29.5) m.y.a. (Masson & Kadereit 2013).
Chenopodioideae s.l. probably originated in Eurasia, perhaps in environments close to the shore, with subsequent movement around the northern hemisphere and then into the southern hemisphere (e.g. Hohmann et al. 2006; Kadereit et al. 2010, 2012). For instance, there have probably been two invasions by C4 Atriplex into North America and then to South America, and two invasions of Australia (Kadereit et al. 2010). Atriplex radiated in Australia in and after the late Miocene (Prideaux et al. 2009; Kadereit et al. 2010); evolution of the C4 clade in the New World probably started a little earlier.
Ecology & Physiology. Amaranthaceae include some 500 species with C4 photosynthesic syndrome, one third of all BLA species with the syndrome and far more than in any other BLA clade (Sage et al. 2012). There are several types of C4 photosynthesis with ca 17 different kinds of leaf anatomy in the family and probably 15 or more independent acquistions of this photosynthetic pathway, perhaps with reversals (e.g. Pyankov et al. 2001; Kadereit et al. 2012). Two thirds of these acquisitions are in the old Chenopodiaceae (Pyankov et al. 2001; Kadereit et al. 2003, 2012; Sage et al. 2007, 2011; Kadereit & Freitag 2011). Within North American Atripliceae there has been a single origin of C4 photosynthesis within Atriplex s. str. (Zacharias & Baldwin 2010).
The first acquisition of C4 photosynthesis in Amaranthaceae can be dated to the early Miocene ca 24 m.y.a., the age of a major C4 clade in Atriplex can be dated to 14.1-10.9 m.y., and other acquisitions may be a quarter of that age or less (Kadereit et al. 2003; Kadereit et al. 2010; Kadereit & Freitag 2011: Christin et al. 2011b for many dates), however, dates of the first acquisition in Kadereit et al. (2012) are a little earlier (47-22 m.y.a.) at the Eocene/Oligocene boundary.
Many Amaranthaceae-Chenopodioideae in particular are halophytes and include a number of C4 species (Jacobs 2001; Sage 2002); of the ca 380 halophytic species, the largest concentration in flowering plants, 43% are C4 plants (Flowers & Colmer 2008). Kadereit et al. (2012) note this connection between the acquisition of C4 photosynthesis and salt tolerance; adaptations to salt tolerance, involving succulence and also drought tolerance, perhaps on the coasts or Eurasia in the Eocene, may have facilitated the subsequent adoption of C4 photosynthesis in chenopods. Compared with grasses, there are relatively few origins of salt tolerance (Kadereit et al. 2012; Bennett et al. 2013).
Many succulent chenopod C4 halophytes grow in the Irano-Turanian region (Ogburn & Edwards 2010) and they make up a major element of the vegetation there. In the rather cold Gobi deserts 15-17% of the species are C4 plants (they are only 3.5% of the total Mongolian flora), yet they contribute 30-90% of the biomass there (Vostokova et al. 1995; Pyankov et al. 2000). Over 50% of the total C4 flora is Amaranthaceae s.l., and is made up of fast-growing C4 chenopods (there are also some Polygonaceae), some of which are arborescent. A similar combination of plants also dominates the halophytic vegetation of the Central Asian Turanian deserts (Winter 1981); these are somewhat warmer than the Gobi deserts. Some of these C4 plants get quite large, Haloxylon aphyllum attaining 10 m in height with a trunk 1 m across (Winter 1981). Succulent C3 chenopods are common in the Gobi in true desert conditions, and also in moist, saline soils (Pyankov et al. 2000).
Aridification in Australia began early in the Miocene ca 22 m.y.a., and the halophytic Camphorosmeae (145 of 147 species) radiated there ca 7.5 m.y.a. (Cabrera et al. 2012). C4 taxa like Atriplex diversified in Australia; the genus was probably a major item in the food of the extinct giant (ca 230 kg) kangaroo Procoptodon goliah (Prideaux et al. 2009; Kadereit et al. 2010). See also Clade Asymmetries.
C4 morphologies are notably diverse. In at least four Suaedeae s.l. all the different elements of C4 photosynthesis are to be found within a single cell, and although there is no conventional Kranz anatomy, the chloroplasts involved in different parts of the carbon fixation process are distinct and spatially segregated, a condition that has evolved independently at least twice (Kapralov et al. 2006: Bienertia, Suaeda). Partitioning of the plastids within the cell is maintained by the distinctive organization of the cytoskeleton (Chuong et al. 2006), although there is plasticity induced by the light environment (Lara et al. 2008). The different plastids may be either proximal and distal (with respect to adjacent veins) in elongated cells, or peripheral and central (most chloroplasts, C3 - Beinertia: Offerman et al. 2011). For details of the evolution of enzymes involved in C4 photosynthesis in Alternanthera, where there are also C2 intermediates, see Gowik et al. (2006). There are summary comparisons of the chloroplast types of C3 and C4 taxa in Koteyeva et al. (2011b), and comparisons of two C4 species in Koteyeva et al. (2011c).
Pollination Biology & Seed Dispersal. In Chenopodioideae s.l. in particular the perianth may become accrescent and envelop the fruit, being variously winged or spiny and involved in seed dispersal (e.g. Cabrera et al. 2009).
Plant/Animal Interactions. Cecidomyiid midges (Asphondylia) form galls on chenopods like Sarcocornia and Tecticornia in Australia; fungi also live in the galls, although the relationshp between the fungi and the midge larvae (the former are food for the latter?) is unclear (Teresa Lebel, pers. comm.).
Bacterial/Fungal Associations. Although the family is apparently largely without mycorrhizae, vesicular-arbuscular mycorrhizae have been reported from chenopods in the Red Desert of Wyoming - but only on native taxa and under undisturbed conditions (Miller 1979); c.f. also Zygophyllaceae.
Chemistry, Morphology, etc. For a discussion about the cortical vascular system, see Fahn and Arzee (1959) and Beck et al. (1982). Stem collenchyma is well developed; there are nucleated xylem fibres (Rajput 2002). Stem-borne roots of Polycnemum seem to have a superficial cork cambium (Heklau et al. 2012).
The flowers of Chenopodioideae s.l. show a considerable amount of variation, partly because of the involvement of the perianth in fruit dispersal, and partly because the flowers may be quite reduced. In the reduced perianth of the Australian Tecticornia (Salicornioideae) the odd member is abaxial (for floral development, see Shepherd et al. 2005b; also Flores-Olvera et al. 2008; the flowers of Beta become semi-inferior during development). Flores-Olvera et al. (2011) found that the "bracteoles" enveloping the flower and fruit in some Atripliceae were in fact modified perianth members.
Pollen of Amaranthaceae (inc. Chenopodiaceae) is fairly homogeneous (Nowicke 1975; Skvarla & Nowicke 1976), both having a similarly thickened tectum, apertures with reduced pointed flecks of exine underlain by lamellar plates, and a thickened endexine; Pseudoplantago has cuboid pollen. However, there is quite a bit of variation beyond this (e.g. Borsch 1998; Borsch & Barthlott 1998). Müller and Borsch (2006c) discuss the evolution of the distinctive stellate pore ornamentation of the pollen of some Amaranthaceae s. str. - there are several independent gains and losses.
2-carpellate members of the family usually have collateral carpels, but occasionally they are superposed. The chalazal region of the ovule is more or less digested by the embryo sac in at least some Amaranthaceae - and this is also once recorded from Nyctaginaceae (Maheshwari 1950).
All in all, Amaranthaceae are morphologically heterogeneous. Some problem taxa: Pleuropetalum (leaves spiral; inflorescence racemose; P 5; A 8, connate basally; G [5-6], several basal ovules/carpel, fruit initially fleshy; n = 8, 9 - A paired in development [Ronse Decraene et al. 1999]), in Amaranthoideae (Townsend 1993).
Additional general information can be found in Eliasson (1988: Amaranthaceae), Robertson (1981: Amaranthaceae), Kühn (1993: Chenopodiaceae), Townsend (1993: Amaranthaceae), and Judd and Ferguson (1999: Chenopodiaceae). See also Blunden et al. (1999: betaine distribution, very common and widespread), Hegnauer (1964, 1989: chemistry), Rajput (2002) and Carlquist (2003c) anatomy, Hakki (1972, 1973: floral morphology, embryology), Meunier (1890), Kajale (1940, 1954), Wilms (1980), and Naidu (1984 and references), ovules and seeds, Shepherd et al. (2005b: fruits and seeds), Sukhorukov (2007, 2008: fruit wall anatomy), and Acosta et al. (2009: inflorescence morphology); Flores Olvera et al. (2006) and Tsymbalyuk (2008) provide information on pollen.
Phylogeny. Cuénoud et al. (2002) found Amaranthaceae s. str. to be monophyletic, with very strong (97%) support, and Chenopodiaceae s. str. were perhaps monophyletic, but the branch collapsed in a strict consensus tree; the sampling was moderately good, but only one gene - matK - was analysed. In an extensive rbcL analysis, much of the old Chenopodiaceae were again monophyletic, but with little bootstrap support, ditto the old Amaranthaceae (incl. Polycnemoideae), while Betoideae were paraphyletic (G. Kadereit et al. 2003). Other studies suggest paraphyly of Chenopodiaceae and sometimes even potential polyphyly of Amaranthaceae (Pratt 2003; Pratt et al. 2001). In an analysis of matK/trnK sequences, Müller and Borsch (2005b, c), Polycnemum and Nitrophila (100% support) were sister to the rest; they may have ordinary secondary thickening (but see Heklau et al. 2012; Masson & Kadereit 2013). Masson and Kadereit (2013) provide a phylogeny of the subfamily. The clade [other Amaranthaceae + Chenopodiaceae] had <70% bootstrap support and still lower PP values, Amaranthaceae s. str. had 100% support and the Chenopodiaceae s. str. again <70% support yet 1.0 PP.
Within Amaranthaceae s. str. - at least some flowers imperfect - Bosea and Charpentiera were successively sister to the rest, but Amaranthoideae, Amarantheae and Amarathineae were paraphyletic (e.g. Ogundipe & Chase 2009). Amaranthus is sister to Beta, etc., in ORF 2280 phylogenies, and this whole group is in turn sister to [Celosia [(Celosieae), Froelichia, etc. + Gomphreneae/Gomphrenoideae] (uénoud et al. (2002). Gomphrenoideae are monophyletic, and have unilocular, monothecal anthers and metareticulate pollen, the mesocolpium being raised (see Downie et al. 1997); the filaments are connate at least basally, pseudostaminodia alternate with the stamens, and bracts and perianth are very scarious (Sánchez del-Pino 2007). Within Gomphrenoideae are the iresinoids (Iresine should be circumscribed broadly), and the [gomphrenoids (Gomphrena is polyphyletic) + alternantheroids (Alternanthera is monophyletic)] (Sánchez del-Pino 2007; Sánchez del-Pino et al. 2009). The monophyly of Alternanthera has been confirmed, and C4 photosynthesis seems to have originated once here (Sánchez del-Pino et al. 2012)
Relationships within Chenopodioideae Burnett s.l. are being reworked because the often highly reduced and modified flowers and fruits have been difficult to understand and interpret, hence leading to unsatisfactory taxon delimitations. Relationships between Dysphanieae Pax (plant aromatic, with stalked or subsessile glands), Atripliceae Duby (inc. Chenopodieae), Axyrideae and Anserineae (inc. Spinacieae) are unclear, although the tribes seem to be monophyletic (Fuentes-Bazan et al. 2012b for a summary). For relationships in the Australian Tecticornia (Salicornioideae) and its relatives, see Shepherd et al. 2004, 2005a). Cabrera et al. (2009) looked at relationships in the Australian Camphorosmeae, to be included in Salsoleae. Kadereit et al. (2010) examined relationships in Atripliceae, and Chenopodium as included there turned out to be polyphyletic, similarly, Fuentes-Bazan et al. (2012a) found that Atriplex and other genera were nested within Chenopodium s.l. - in fact, members of four erstwhile tribes were intermingled. For Atripliceae, see also Zacharias and Baldwin (2010: North American taxa). Other studies on groups of Chenopodiaceae sensu stricto: Schütze et al. (2003: Suaedoideae), G. Kadereit et al. (2005: Australian chenopods, 2006: Salicornioideae), Akhani et al. (2007: Old World Salsoleae [Salsoloideae - mostly C4, embryo spiral, perisperm ± 0; seed compressed]), Hohmann et al. (2010: Betoideae), and Wen et al. (2010: Salsoleae s.l. - monophyletic).
Amaranthaceae s. s. have cuticle waxes lacking platelets; scarious bracts and perianth, and the filaments are often connate; n = (6-)8-9(-13, etc). The embryogeny is chenopodiad[!]. Chenopodiaceae sensu stricto quite commonly have isoflavonoids; cuticle waxes as platelets; bracts and P ± fleshy, pink to red; fruit rarely circumscissile; n = 9; 300 bp deletion in chloroplast DNA inverted repeat.
Classification. Within Gomphrenoideae, Iresine should be circumscribed broadly and Gomphrena is polyphyletic (Sánchez del-Pino 2007; Sánchez del-Pino et al. 2009). Some of the extreme halophytic genera are morphologically much modified, and generic limits are difficult; there is much variation in fruit and seed, the former in particular involving apparent adaptations for dispersal, and genera based on this variation are not holding up (Shepherd & Wilson 2007; Kadereit & Freitag 2011).
Kadereit and Freitag (2011) have begun to separate out subfamilies within the chenopod part of the clade, but the end result of this exercise is unclear. Cabrera et al. (2009) found generic problems in the Australian Camphorosmeae (= Salsoleae s.l.) Maireana being in a particular mess. Zacharias and Baldwin (2010) divided the C3 North American Atriplex and relatives, which are quite variable, into a number of genera, while Fuentes-Bazan et al. (2012) has made the needed nomenclatural changes in Chenopodium s.l..
For Microtea, sometimes included here, see Microteaceae above.
Synonymy (A = Amaranthaceae s. str., C = Chenopodiaceae s. str.): Achyranthaceae Rafinesque (A), Atriplicaceae Jussieu (C), Betaceae Burnett (C), Blitaceae Kuntze (C), Celosiaceae Martynov (A), Chenopodiaceae Ventenat, nom. cons., Corispermaceae Link [status] (C), Deeringiaceae J. Agardh (A), Dysphaniaceae Pax, nom. cons. (C: cuticle waxes absent), Gomphrenaceae Rafinesque, Polycnemaceae Menge (C), Salicorniaceae Martynov (C), Salsolaceae Menge (C), Spinaciaceae Menge (C)
[Stegnospermataceae [Limeaceae [[Lophiocarpaceae [Hypertelis [Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]]: ?
STEGNOSPERMATACEAE Nakai Back to Caryophyllales
Woody, ± scandent; successive cambia +; true tracheids +; plant glabrous; leaves fleshy; inflorescence racemose; C (2-)5; A (5) 8-10, connate basally; nectaries in depressions at base of G; G [2-5], opposite, placentation becoming free-central, stigma/styles ± spreading; ovule 1/carpel, basal, epitropous, amphitropous; fruit a capsule; seeds arillate, exotesta ± palisade, unlignified, endotegmen enlarged, persistent; n = ?
1[list]/3. Central America, the Antilles (map: from Bedell 1980). [Photo - Fruit]
Chemistry, Morphology, etc. Like Caryophyllaceae, there are special cells in the wood that contain sphaerites; there is only diffuse axial xylem parenchyma. There is no nucellar cap. Are the seeds endospermic?
For more information, see Friedrich (1956: c.f. carpel position), Hofmann (1977: general), Bedell (1980: general), Horak (1981) and Carlquist (2012c), secondary thickening, Narayana and Narayana (1986: embryology) and Rohwer (1993a: general).
Previous Relationships. Stegnospermaceae have often been included in Phytolaccaceae. The two look rather similar, and have a somewhat similar gynoecium, but they are most obviously distinguishable by their flowers which have petals. They also have pollen with a prominent foot layer and massive endexine - this is thin in Phytolaccaceae. The ovules are epitropous, while in pluricarpellate Phytolaccaceae they are apotropous (Rogers 1985).
[Limeaceae [[Lophiocarpaceae [Hypertelis [Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]: ovules apotropous.
LIMEACEAE Reveal Back to Caryophyllales
Herbs or subshrubs; "unpigmented", ?chemistry otherwise?; cork?; (secondary thickening normal); nodes?; leaves spiral; inflorescence leaf-opposed or not; P quincuncial; "C" +, clawed (0), A 5(-7), basally connate, all opposite P; G , septate, styles 2; ovule 1/carpel, pendulous; antipodal cells persist; fruit a schizocarp; seeds brown; testa with cells in rows along the dorsal junction; n = 9.
1/21. Southern Africa (most species), to Ethiopia, S. Asia (map: from Culham 2007; esp. Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011).
Chemistry, Morphology, etc. Petaloid staminodes are described as coming from the base of the outer stamens; the nature of the gynoecium is unclear, but there are certainly two stigmas and sometimes (at least) clearly two styles that are very close together at the base (e.g. Jeffrey 1961).
For further information, see Sharma (1963: floral morphology), Hofmann (1973: flower, growth), Behnke (1976) and Behnke et al. (1983a(, both plastids, M. Endress and Bittrich (1993: general, as Molluginaceae), and Hassan et al. (2005a: seed coat).
Previous Relationships. Another member of the old Molluginaceae (M. Endress & Bittrich 1993).
[[Lophiocarpaceae [Hypertelis [Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]: (wide-band tracheids +); sieve tube plastids with globular crystalloids.
Evolution. Physiology & Ecology. Wide-band tracheid pith cells in succulents (e.g. Aizoaceae, Cactaceae, Portulacaceae) are also found in the leaf away from the midrib in Aizoaceae; bands are narrow but very tall (= "wide"), so the cell lumen is locally very narrow (Mauseth et al. 1995 - similar in Hectorella [Montiaceae] - Carlquist 1998b). In a recent study of Ariocarpus fissuratus (Cactaceae), it was found that as the rays expanded these tracheids could contract, so allowing the whole root to contract, and the plant remained closer to the rocky ground where the temperatures were cooler (Garrett et al. 2010).
Chemistry, Morphology, etc. Limeaceae, Cactaceae and "Portulacaceae" have cells in rows along the dorsal junction of the seed.
[Lophiocarpaceae [Hypertelis [Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]]]: ?
Phylogeny. Corbichonia (Lophiocarpaceae) and most of Hypertelis (one species is in Molluginaceae) were well supported as successive sister clades at the base of this clade (Christin et al. 2011a); the whole clade badly needs study to establish relationships along its backbone. Aizoaceae and Nyctaginaceae seem to be the only fixed entities around here.
LOPHIOCARPACEAE Doweld & Reveal Back to Caryophyllales
Anthocyanins?; inflorescence a raceme with 3-flowered cymules or a leaf-opposed cyme [Corbichonia, inflorescence evicted]; K/P quincuncial, C 0 [Lophiocarpus] or several, staminodial, ± connate; A 4 [Lophiocarpus], several, centrifugal; tapetal cells 2-3-nucleate; G , 1-locular, or  [Corbichonia], carpels opposite sepals, placentation axile [Corbichonia]; ovule single [per flower], or many/carpel [Corbichonia], parietal tissue to 3 cells across; fruit an achene or capsule; seed arillate [Corbichonia]; exotestal cells radially elongated; n = ?
2 [list]/6. Africa, esp. S.W. Africa, to western India. Lophiocarpus rather weedy (map: approximate, from floras and florulas; Jeffrey 1961; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
Chemistry, Morphology, etc. These two genera are florally very different, as is clear from the characterization above. For Corbichonia flowers, see Ronse de Craene (2007), for embryology, see Narayana (1962a) and Narayana and Lodha (1963: as Orygia, ovules shown as almost anatropous). For some general information, see Adamson (1958) and Hofmann (1973).
Previous Relationships. Previously included in Phytolaccaceae (Lophiocarpus: Rohwer 1993) and Molluginaceae (Corbichonia: M. Endress & Bittrich 1993).
[Hypertelis [Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]]: ?
HYPERTELIS Back to Caryophyllales
Herbs or subshrubs; anthocyanins +; cork?; secondary thickening?; (stout glandular hairs +); leaves ± fasciculate, linear, terete, stipules adnate to base, ± sheathing; inflorescence pseudo-umbellate, pedunculate; P 5, sepal- to petal-like [the latter, 3-4]; A (3-)5-15(-20); G [3-5], opposite sepals, placentation axile, style 0; ovules many/carpel; fruit a membranous capsule or schizocarp; seeds operculate; n = 8.
1/8. South Africa (most), to Ethiopia, Madagascar, and St Helena (map: from Adamson 1958a; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011).
Chemistry, Morphology, etc. The inflorescence is interpreted as beuing terminal and cymose (Hoffmann 1973). In bud, the perianth members enclose the rest of the flower and are sepal-like; in the open flower three or four expand and are petal-like, the anthers and stigmas also being brightly colored.
For further information, see Behnke et al. (1983a: sieve tube plastids), M. Endress and Bittrich (1993: general, as Molluginaceae), Adamson (1958a: general, South African species), and Hassan et al. (2005a: seed coat).
Phylogeny. The exclusion of Hypertelis spergulacea (see Molluginaceae) makes morphological sense.
Previous Relationships. Another member of the old Molluginaceae (M. Endress & Bittrich 1993).
[Barbeuiaceae [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]]: successive cambia +.
BARBEUIACEAE Nakai Back to Caryophyllales
Lianes; betalains?; libriform fibers, diffuse axial parenchyma, true tracheids +; sieve tube plastids with polygonal crystalloids[!]; cortical fibres +; druses +; leaves spiral; P 5; A many; pollen tricolporoidate; G , septate; ovule 1/carpel; fruit a loculicidal capsule; seeds 1 or 2, arillate, testa cells elongated, with sinuous anticlinal walls; n = ?.
1[list]/1: Barbeuia madagascariensis. Madagascar (map: from Culham 2007).
Chemistry, Morphology, etc. The plant dries black. See Hofmann (1977: general), Rohwer (1993a: general, under Phytolaccaceae) and Carlquist and Schneider (2000: anatomy).
[Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]]: soluble oxalate accumulation; raphides +; anther wall from both secondary parietal layers.
For soluble oxalate accumulation, see Zindler-Frank (1976).
AIZOACEAE Martynov, nom. cons. Back to Caryophyllales
Leaf succulents; growth sympodial; CAM +; C-glycosylflavonoids -; cork from inner cortex or endodermis; wood storied, wood rayless; fibres ± in bands; wide-band tracheid pith cells; cuticular waxes as ribbons or rodlets; stomata also para- and anisocytic; leaf trace bundles forming reticulum in cortex; leaves opposite, lamina with bladder-like cells on epidermis, leaf base broad, membranous; inflorescence with well-developed bracts/bracteoles; hypanthium +; P coloured adaxially and basally, often with subapical abaxial appendage ["horn"]; nectary annular, on hypanthium; A often many, centrifugal, primordia 5, wall ?ordinary, tapetal cells 2-nucleate; pollen tricolp(oroid)ate; G septate; ovule with parietal tissue ca 3 cells across; exotesta ± palisade, or tangentially elongated; x = 8.
123[list]/ca 2035 - four subfamilies below. Esp. southern Africa, also Australia, etc., tropical and subtropical, arid. [Photos - Collection.]
1. Sesuvioideae Lindley
Nodes also 3:3; petiolar stipules +; prophylls often prominent; A 1-5, alt. P, or many, primordia opposite P, or development rather chaotic; G (1-)[2(-5]), 2-many ovules/carpel; capsule circumscissile, (winged or compound fruit, fused with spiny bracts - Tribulocarpus); seeds arillate (not).
4/41: Trianthema (32), Sesuvium (12). Tropics and Subtropics; Sesuvium portulacastrum is pantropical on beaches (map: see Fl. Austral. 4. 1984; Hartmann 2001a, b; Hartmann et al. 2011; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. 4: 2003). [Photos - Habit, Flower.]
Synonymy: Sesuviaceae Horaninow
[Aizooideae [Mesembryanthemoideae + Ruschioideae]]: inflorescence often not distinct from vegetative plant, bracteoles foliaceous; A primordia alternating with P; G opposite P; fruit loculicidal, a hygrochastic capsule; seeds brown.
Bladder hairs with large terminal cell and multicellular stalk[?]; accessory lateral branches + [?]; (A 10), nectary apically on the hypanthium; G [2-10], to inferior; ovule 1/carpel, apical, apotropous, or basal, many ovules; (fruit septicidal - Gunniopsis; indehiscent - Tetragonia); seeds upright [?], (cell walls of seed coat little thickened).
7/135: Tetragonia (85). Drier parts of S. Africa, also Australia (Gunniopsis), few N. Africa and Asia Minor, N. America, etc. (Aizoon) (map: see Frankenberg & Klaus 1980; Fl. Austral. 4. 1984; Hartmann 2001a, b). [Photo - Flower]
Synonymy: Galeniaceae Rafinesque, Tetragoniaceae Lindley
[Mesembryanthemoideae + Ruschioideae]: leaves very succulent; hypanthium 0; P green, sepal-like, "C" staminodial, many; G more or less inferior, nectary interrupted; x = 9.
3. Mesembryanthemoideae Ihlenfeldt, Schwantes & Straka
Distinctive alkaloids [in Phyllobolus, etc.] +; wide-band tracheids 0; cortical bundles +; (stem succulents; succulent persistent green cortex in stem); stomata on both stem and leaf transversely (vertically) oriented; flowers 4-5-merous; (filaments connate), nectary hollow and ± shell-shaped [koilomorphic] (flat); G [(3-)4-5(-6)], placentation axile; parietal tissue 7-9 cells across, in radial rows or not; expanding keels of fruit purely septal; (n = 18, 27).
1-11/100. S. Africa, a few species also W. South America, Australia, N. Africa, the Mediterranean and the Near East, naturalised in W. North America (map: see Fl. Austral. 4. 1984; Pascale Chesselet, pers. comm. 2004).
Synonymy: Mesembryaceae Dumortier, Mesembryanthaceae Philibert, nom. cons.
4. Ruschioideae Schwantes
Leaves flat; inflorescence often distinct; nectary flat, annular, broad; G [(3-)5-15(-25)], placentae basal or parietal; expanding keels of fruit largely valvar, not reaching centre of fruit, wih covering membranes (map: Pascale Chesselet, pers. comm. 2004).
Annuals to perennial; (fruit schizocarpic).
7/11[!]. South Africa, mostly southwest.
Annuals; nectary segmented.
1/10. Southwest South Africa.
4C. The Rest.
Wide-band tracheids +; bladder cells 0; leaves (spiral), lamina trigonous or terete, vernation curved to flat; filaments (basally connate), papillate or hairy at base, nectaries usu. crest-like [lophomorphic, bulging]; (chloroplast rpoC1 intron lost), ARP gene duplicated.
Ca 96/ca 1565: Ruschia (290-350), Conophytum (87-290), Lampranthus (180-220), Delosperma (155-165), Phyllobolus (150), Drosanthemum (100-110), Psilocaulon (65), Antimima (6-60), Lithops (37-50+). Southern Africa, esp. the western coastal Succulent Karroo. [Photos - Flower; Flower.]
Evolution. Divergence & Distribution. Klak et al. (2004) suggest that the radiation in Ruschioideae in S.W. Africa, at least, is both recent (3.8-8.7 m.y.a.) and very fast; however, the estimates in Arakaki et al. (2011) are about twice as old. Interestingly, the "meganiche" dominated by the family - rather arid winter-rainfall areas with moderate temperatures - may be only some 5 m.y. old (Ihlenfeldt 1994a).
Ecology & Physiology. Aizoaceae, in particular Mesembryanthemoideae and Ruschioideae, dominate much of the Succulent Karoo of southwestern Africa, making up more than 50% of the species and up to an astounding 90% of the biomass. Members of these groups may be either salt tolerant or drought avoiders, and it is unusual to have this variation in quite closely related species (Ogburn & Edwards 2010). Edaphic specialization - soils can vary considerably locally - seems also to be involved in the diversification of the family (Ellis & Weis 2006).
C4 photosynthesis occurs in some members of this clade, especially Sesuvioideae (Sage et al. 1999); some origins may be as much as (27-)22.1(-17.2) m.y.a., others are much younger (Christin et al. 2011b).
Variation in vegetative characters such as leaf size and shape and internode elongation is considerable (Ihlenfeldt 1994a). Although a distinction is sometimes made between plants with foliaceous bracts or bracteoles in which the inflorescence is not distinct from the rest of the plant, and plants with smaller bracts and distinct inflorescences (e.g. Hartmann 1993), it is unclear to me what the real growth characters are and where they go on the tree. A number of taxa have bladder-like cells on the leaf surface ("idioblasts") that may be involved with water uptake from dew or mist. Other taxa may have massively-thickened outer cell walls that contain layers of calcium oxalate crystals (e.g. Ihlenfeldt & Hartmann 1982). In addition, individual cells may be variously papillate or the surface otherwise sculpted and/or with epicuticular waxes, the stomatal openings may be deeply sunken, etc. (e.g. Ihlenfeldt & Hartmann 1982; Hartmann 2002; Opel 2005a).
The leaves of many Ruschioideae are more or less flush with the surface of the ground; they can be almost invisible in the stony habitats in which they grow, being greyish or brownish and looking like pebbles except when they flower - hence "flowering stones". The exposed surfaces of the leaves sometimes have distinctive "windows". Within the single genus Lithops the window patterning may reflect venation reticulation or the position of huge, tannin-containing cells (Korn 2011). These leaves are prophylls or bracteoles, the flower is terminal, and renewal shoots, the next flowering units, develop in the axils of the leaves (Hartmann 2004, 2006 for a summary). In some species of Conophytum the leaves are almost completely connate except for a slit across the top out of which the flower and next pair(s) of leaves appear.
The leaves of core Ruschioideae, i.e., not including Drosanthemeae and Ruschieae, are cylindrical or trigonous, not more or less flattened (Klak et al. 2004; Chesselet et al. 2004) and they lack the bladder-like epidermal cells of the rest of the family. A duplication of the ARP gene, involved elsewhere in leaf development, is correlated with the diversification of core Ruschioideae, and the ARP gene may be involved in the evolution of the diverse leaf morphologies of this group, although this idea is currently based on a simple correlation (Illing et al. 2011, c.f. the phylogenetic interpretation there).
Pollination Biology & Seed Dispersal. Aizoaceae in the drier areas of southwestern Africa are much visited by bees, which also visit Asteraceae there (Kuhlmann & Eardley 2012) - the two do have grossly similar flowers.
Straka (1955), Ihlenfeldt (1983) and Hartmann (1988) have described the intricate morphology of the capsules of the [Aizooideae [Mesembryanthemoideae + Ruschioideae]] clade, which are often hydrochastic. There are septal keels that reach from the central axis to the valve tips that expand when they absorb water. Seed dispersal is by "jet action" using the kinetic energy of falling raindrops (= ombro[hydro]chory: Parolin 2006), but depending on the details of the capsule morphology, seeds may be dispersed different distances. The ease of dispersal of the seeds is inversely correlated with the distance the seed travels - if easily ejected, the seeds are not propelled far. In a few taxa the fruits are dispersed as entire mericarps. There is also considerable variation in the establishment "strategies" of the seeds. Many Sesuvioideae, with more conventional fruits, have arillate seeds and are myrmecochorous (Lengyel et al. 2009).
Apatesieae and Dorotheantheae are successively sister to the remainder of Ruschioideae, they are not very speciose. The much more speciose core Ruschioideae often have crest-like (lophomorphic) nectaries and hygrochastic capsules with a distinctive anatomy (for which, see Kurzweil 2006) that release only a few seeds at a time.
Chemistry, Morphology, etc. Studies of the wood anatomy of Aizooideae and Sesuvioideae are needed to clarify wood evolution there (Carlquist 2007a); see Rajput and Patil (2008) for a study of vascular development in Sesuvium portulacastrum.
The petal-like basal part of the perianth in Sesuvioideae is equivalent to the sheathing vegetative leaf base and the apical "horn" to the rest of the leaf, rather as in monocot leaf development (c.f. Vorlaüferspitze!); the petal-like B floral genes were not expressed in the basal part, nor were they in the petal-like staminodes of Aizooideae and Ruschioideae (Brockington et al. 2012; for the latter c.f. in part Frohlich et al. 2007). The androecium may arise as a ring meristem or as five separate primordia. Smets (1986) records the presence of a receptacular nectary disc. Although Niesler and Hartmann (2007) suggested that the correlation of nectary morphology with major clades was not that strong, finding more or less flat nectaries in Glottiphyllum (Ruschioideae), they occur in the two basal clades in that subfamily. Hartmann (1993) recorded a nucellar cap in Aizoaceae, but by this he meant the radially elongated cells of the nucellar epidermis. Aptenia has a wet stigma.
For more information, Meunier (1890: ovules and seeds), Schwantes (1957: esp. fruit dehiscence), Hegnauer (1964, 1989: chemistry), Hofmann (1973: morphology), Haas (1976: esp. flower and fruit), Bittrich (1986: general, esp. Mesembryanthemoideae), Hartmann (1993: general), Leins and Erbar (1993: floral development), Klak and Linder (1998) and Klak et al. (2006: esp. stomata), Landrum (2001: wide-band tracheids), Niesler and Hartmann (2004: some leaf morphology), Chesselet et al. (1995, 2002: esp. information on Mesembryanthemoideae and Ruschioideae), Klak (2010: general), Hartmann and Niesler (2009: detailed survey of nectaries) and Interactive Mesembs. The books edited by Hartmann (2001a, b) include thousands of photographs.
Phylogeny. I follow Klak et al. (2003) for basic groupings in the family; Aizoaceae s. str. (e.g. Chesselet et al. 1995) would seem to be paraphyletic. Tribulocarpus, which used to be in Tetragonioideae (for which, see Aizooideae), is sister to the other Sesuvioideae, in which it is included here (Klak et al. 2003; Thulin et al. 2012a); it has an indehiscent fruit and so hardly surprisingly lacks arillate seeds. For a phylogeny of Sesuvioideae, see Hassan et al. (2005b). Tetragonia is embedded in Aizooideae (Klak et al. 2003), however, it has wood rays, it lacks the bands of xylem fibres of other Aizoaceae, and there is vasicentric parenchyma adjacent to these fibres (Carlquist 2007).
Apatesieae and Dorotheantheae are successively sister to the remainder of Ruschioideae (see above for details of morphology, etc.; Klak & Bruyns 2012 for a phylogeny of Dorotheantheae). The remainder, core Ruschioideae, have also lost the chloroplast rpoC1 intron (Thiede et al. 2007) - c.f. Cactoideae! See Opel (2005a) for leaf anatomy and Opel (2005b) for a morphological phylogenetic analysis of Conophytum (Ruschioideae); current estimates of species numbers for this genus range from 87 to 290.
Classification. There is a combined [list] of genera recognised in Mesembryanthemoideae and Ruschioideae, but generic boundaries are uncertain, both species and genus limits are difficult. In the early twentieth century Mesembryanthemum included the whole of the Ruschioideae and Mesembryanthemoideae, and until recently the Mesembryanthemoideae, by far the smaller of the two subfamilies, was divided into numerous genera. However, Klak et al. (2007) in a comprehensive study of the subfamily, obtained quite detailed phylogenetic resolution within it. Mesembryanthemum itself, although quite a small genus, was polyphyletic, and any attempt to maintain current genera would, Klak thought, have caused the recognition of numerous and often poorly characterised taxa; only one genus was recognised. This decision may have to be revisited, since others think that clades there can be characterised (V. Bittrich, pers. comm.; Liede-Schumann & Hartmann 2009).
Hammer in 1993 noted that there were then about 1,800 known populations of Conophytum (Ruschioideae) - for which there were 450 names; current estimates of species numbers for this genus range from 87 to 290. For a general account of Lithops, see Cole and Cole (2005); Kellner et al. (2011) looked at genetic differentiation in the genus in the context of morphology and geography. For an infrageneric classification of Drosanthemum, see Hartmann (2007).
[Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]: ovule 1/carpel, basal; ORF 2280 sequence similarity, 210 bp deletion in chloroplast genome.
Phylogeny. Douglas and Manos (2007) found only moderate support for the monophyly of Nyctaginaceae and vanishing little support for the monophyly of Phytolaccaceae (including Sarcobataceae). Similar relationships were found by Brockington et al. (2009), but with Gisekia strongly supported as sister to the whole clade.
Both Phytolaccaceae-Rivinioideae and Nyctaginaceae have gynoecia made up of a single carpel (Cuénoud et al. 2002), and the single carpels of Mirabilis and Rivina look remarkably similar to each other (Leins & Erbar 1994). However, if Sarcobataceae are placed somewhere around here, perhaps even within the already polymorphic Phytolaccaceae, its carpel number is a reversal...
Classification. Family limits in this area may need adjustment;
GISEKIACEAE Nakai Back to Caryophyllales
Prostrate herb; successive cambia 0; C4 photosynthesis +; leaves opposite; inflorescence leaf-opposed, dichasial to subumbellate; P 5, quincuncial; A 5(-15), alternating with P; G (3-)5(-15), pseudapocarpous, opposite P, styluli +; ovule 1/carpel, parietal tissue 2-3 cells across, nucellar cap 2-3 cells across, cells of nucellus expanded radially, funicle short; antipodal cells ± persistent; plant heterocarpic, some mericarps ± muricate or winged, fruits achenial; exotestal cells tangentially elongated, exotegmic cells also thickened; n = 9.
1/5. Africa, Asia (map: from Culham 2007, modified by Frankenberg & Klaus 1980; Flora Ethiopia Eritrea 2(1). 2000; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011; Flora of China 5).
Evolution. Divergence & Distribution. The maximum age for the evolution of C4 photosynthesis here is (8.4-)4.8(1.2) m.y. (Christin et al. 2011b: s.d.).
Chemistry, Morphology, etc. See Hofmann (1973) for floral morphology, growth, Behnke (1976) and Behnke et al. (1983a) for sieve tube plastids, Gilbert (1993) for a review, Joshi and Rao (1936: suspensor apically curved and beak-like), Narayana (1962a) and Hassan et al. (2005a) for ovule and testa morphology, and Narayana and Narayana (1988) for a little chemistry.
Phylogeny. "Discordant" wherever it is put, but in some phylogenies to be placed with Phytolaccaceae-Rivinioideae (see Cuénoud et al. 2002)...
[Sarcobataceae, Phytolaccaceae, Nyctaginaceae]: ?
SARCOBATACEAE Behnke Back to Caryophyllales
Thorny shrub; cork etc.?; wood rayless; ?stomata; leaves fleshy, sessile; plant monoecious, bracteoles 0; P 0; staminate inflorescence: catkinate; flowers with peltate scales ["bracts"]; A 1-4, anthers much longer than filaments; pollen pantoporate, pore margins raised; carpellate inflorescence: flowers single; bracteoles connate, tubular, bilobed; G , [?position], style bilobed; funicle?; fruit?; embryo flattened, spiral, green; n = 9.
1/2. S.W. North America, saline habitats (map: from Fl. N. Am. 4: 2003). [Photos - Collection.]
Chemistry, Morphology, etc. Is Sarcobatus really worth placing in a separate family (c.f. Behnke 1997)? Some information is taken from Carlquist (2000a).
Previous Relationships. Sarcobatus used to be included in Chenopodiaceae, but sieve tube plastids with globular inclusions, etc., suggest that it goes somewhere around here (Behnke 1997).
[Phytolaccaceae + Nyctaginaceae]: cork subepidermal; stomata also paracytic; protein bodies in nuclei.
PHYTOLACCACEAE R. Brown, nom. cons. Back to Caryophyllales
Cuticular waxes as platelets; leaves (opposite), lamina vernation conduplicate; inflorescences ± racemose, (leaf-opposed); P 5(-10); styles ± gynobasic; funicular hair-type obturator +; P and A persistent in fruit.
18[list]/65 - three groups below. Tropical and warm temperate, esp. America (map: from Fl. N. Am. 4: 2003). [Photos - Collection.]
Herbs, vines or soft-wooded trees; saponins +; fibers vasicentric; (inflorescence leaf-opposed); P usu. 5; tapetal cells multi-nucleate; G [4-16], (opposite P), styluli gynobasic; G [3-16], often pseudapocarpous; ovules with (outer integument ca 5 cells across), epidermal cells palisade, parietal tissue ca 2 cells across, nucellar cap 3-14 cells across, hypostase +, funicle?, (obturator +); fruit a berry; embryo white; n = 9.
4/31: Phytolacca (25). New World, few in Old World, also weedy (Phytolacca) (map: from Fl. N. Am. 4: 2003; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
Synonymy: Sarcocaceae Adanson
2. Rivinioideae Nowicke
Herbs to trees or lianas; saponins 0; (spines prophyllar); styloids, elongate crystals +; inflorescence racemose, branched or not (flowers terminal - Seguieria); (bracteoles slightly abaxial; (flowers weakly monosymmetric); P 4, (diagonal), (5 - Seguieria); A 4-20, centrifugal, (extrorse - Hilleria); pollen 3-many colpate or 7-many porate, G 1, stylulus +, stigma capitate, or flattened, stigma decurrent down one side, or 0, stigma peniceillatestigma capitate [?always]; outer integument 3-4 cells across [thicker towards chalaza], inner integument ca 2 cells across, parietal tissue 2-18 cells across, nucellar cap ca 2 cells across; fruit samara, spiny, or baccate, indehiscent; exotesta radially elongated, lumen ± obscure to obvious; suspensor massive, (cotyledons spirally folded); n = 18, 54; seedling epigeal, phanerocotylar.
9/13. Southern U.S.A. to South America, the Antilles, Australia, New Hebrides and New Caledonia (Monococcus) (map: from Rohwer 1982; Fl. Austral. 4. 1984; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. 4: 2003).
Chemistry, Morphology, etc. Petiveria and Gallesia smells of onions. Both Monococcus and Petiveria have four perianth parts that are diagonally arranged but their bracteoles are strictly lateral, while the perianth of the other genera is orthogonally arranged and the bracteoles are slightly adaxial (e.g. Vanvinckenroye et al. 1997). Ovules of Petiveria have a nucellar beak.
See also Mauritzon (1934c: embryology), Rohweder (1965: gynoecium), Hegnauer (1969, 1990: chemistry), Nowicke (1969: general, esp. pollen), Hofmann (1977), Ronse De Craene and Smets (1991d), Leins and Erbar (1993), all floral morphology/development, Rohwer (1882, 1993a: general), Carlquist (2000b) and Jansen et al. (2000c), both wood anatomy.
Synonymy: Hilleriaceae Nakai, Petiveriaceae C. Agardh, Riviniaceae C. Agardh, Seguieriaceae Nakai
3. Agdestidoideae Nowicke
Liane; diffuse axial parenchyma, true tracheids +; wood rayless; Ca oxalate crystals 0; cuticle waxes with ± rounded platelets; inflorescence branches cymose; P 4 (5); A 12-16(25), in groups alternating with P; G [(3-)4], seminferior, septate; fruit a 1-seeded achene with sepal-like wings
1/1: Agdestis clematidea. S. U.S.A. to Nicaragua (map: from Fl. N. Am. 4: 2003; Culham 2007).
Chemistry, Morphology, etc. Some information is taken from Hoffman (1994).
Synonymy: Agdestidaceae Nakai
Evolution. Divergence & Distribution. Fossil fruits from the Upper Cretaceous (late Campanian) of Mexico are similar to those of Phytolacca, Cevallos-Ferriz et al. (2008) noting a palisade exotesta and also a palisade layer in the tegmen.
Chemistry, Morphology, etc. Phytolacca is reported, probably incorrectly, to have glucosinolates (Fahey et al. 2001 for literature). The pollen is similar in all subfamilies. The carpels of Phytolacca are initiated in a ring around the apex of the axis (Zheng et al. 2004).
See also Rohwer (1993a: general, Microtea included, see Amaranthaceae here), Hegnauer (1969, 1990: chemistry), Carlquist (2000b: anatomy), Meunier (1890: ovules and seeds), Mauritzon (1934c) and Kajale (1954), both embryology, Rohweder (1965: gynoecium), Nowicke (1969: general, esp. pollen), Hofmann (1977), Leins and Erbar (1993), and Zheng et al. (2010), all floral morphology/development.
Previous Relationships. Gyrostemonaceae, commonly with glucosinolates and now included in Brassicales very close to Resedaceae, have been linked with Phytolaccaceae by some authors in the past...
NYCTAGINACEAE Jussieu, nom. cons. Back to Caryophyllales
Annual herbs to shrubs, often rather weak-stemmed trees, or lianes; (isoflavonoids +); (cork cortical); wood storied, often rayless; (vessel elements with reticulate perforations); leaf wax crystalloids 0; flowers in cymose clusters; P connate, petal-like, lobes induplicate-valvate or contorted; A often connate at the very base; (nectary on receptacle); G 1, stigma asymmetric, expanded, capitate to fimbriate; ovule with short funicle; embryo sac haustorium +; fruit surrounded by persistent P, achene or nutlet; embryo green; n = (8-)11(-13+).
30[list]/395. Tropical to warm temperate (map: see Stemmerik 1964; Fl. Austral. 4. 1984; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. 4: 2003; Culham 2007). [Photo - Fruit, Collection.]
1. Leucastereae Bentham & Hooker
Trees; styloids, etc.; indumentum ± stellate; A 2, 3 (10-20); style thick/0, stigma crest-like; (P accrescent in fruit - Ramisia); embryo hooked.
4/5. S.E. South America, esp. Brasil.
[Boldoeae [Colignonieae, [Bougainvilleae + Pisonieae], Nyctagineae]]: style long, slender.
2. Boldoeae Heimerl
Bracteoles 0; stigma inconspicuous (style 0, stigma fimbriate).
3/3. Mexico to Bolivia, the West Indies.
[Colignonieae, [Bougainvilleae + Pisonieae], Nyctagineae]: (gypsophily); leaves opposite; (involucre +); P bipartite, tube stout, limb thin; A 1-many, of varying lengths; pollen pantoporate, also tricolpate, etc.; basal part of P tube accrescent, often mucilaginous, rest withering; (cotyledons unequal).
3. Colignonieae Standley
P only basally connate.
1/6. Andean South America
[Bougainvilleae + Pisonieae]: outer integument 4-6 cells across, (integument single - 3-6 cells across), parietal tissue ca 4 cells across.
4. Bougainvilleae Choisy
(Lianes, climbing by branch hooks); leaves spiral.
3/16: Bougainvillea (14-18). Central and tropical South America; southwest Africa.
Synonymy: Bougainvilleaceae J. Agardh
5. Pisonieae Meisner
(Testa multiplicative, unstructured [Pisonia]); embryo straight, cotyledons unequal.
7/200: Neea (85), Guapira (70), Pisonia (40). Pantropical, but especially New World.>.
Synonymy: Pisoniaceae J. Agardh
6. Nyctagineae Horaninow
(C4 photosynthesis +); (outer integument 5-7 cells thick - Mirabilis); (endotesta thickened [Mirabilis]); embryo hooked.
11/184: Boerhavia (50), Mirabilis (45). Tropical to warm temperate, esp. herbs and shrubs in arid southwestern North America
Synonymy: Allioniaceae Horaninow, Mirabilidaceae W. Oliver
Evolution. Ecology & Physiology. A xerophytic clade is especially common in S.W. North America, and is noted for its abundance in dry or desert conditions. A number of species also tolerate gypsum-rich soils (esp. Abronia - see Saunders & Sipes 2011), and diversification of the desert clade may have begun in the Oligocene or Miocene (Drummond et al. 2012).
The origin of C4 photosynthesis in Boerhavia and Allionia has been dated to within the last 7 m.y. (Christin et al. 2011b).
Pollination Biology & Seed Dispersal. The single-flowered inflorescences of some species of Mirabilis can look remarkably like individual flowers: The green inflorescence bracts appear to be a calyx, and the brightly-coloured connate perianth looks like a sympetalous corolla. Taxa that flower in the evening or night (hence the common name, the "four o'clock family") are quite common (Douglas & Manos 2007); Nores et al. (2013) summarize pollination biology in the family.
The subepidermal cells of the perianth may produce mucilage when the fruit is wetted, and this is especially notable in disseminules of the xerophytic North American clade. In species like Pisonia the pericarp becomes viscid and very sticky indeed; it is used as bird lime to catch birds.
Bacterial/Fungal Associations. Pisonieae may form ectomycorrhizae with various basidiomycetes (Haug et al. 2005).
Chemistry, Morphology, etc. Carlquist (2004) examined secondary thickening in Nyctaginaceae in detail: there is a lateral meristem that produces secondary cortex to the outside, and to the inside rays, conjunctive tissue, and a succession of vascular cambia, from which the more or less isolated areas of vascular tissue (but not rays) are derived. Hernández-Ledesma et al. (2011) looked at variation within Mirabilis in some detail.
Some Nyctaginaceae (Boerhavinae, Nyctagineae) have pollen grains ca 200 µm long, about the largest in angiosperms outside the aquatic Cymodoceaceae (Alismatales). For necataries in the family, see Nores et al. (2013). The single ovule seems to terminate the apex of the stem (Sattler & Perlin 1982). Abronia has only a single well-developed cotyledon, while the cotyledons of Pisonia and its relatives are unequal in size (and the embryo is straight).
See Woodcock (1929) for ovules, Hegnauer (1968, 1990) for chemistry, Vanvinckenroye et al. (1993) for floral development, and Bittrich and Kühn (1993) for general information.
Phylogeny. The South American Leucastereae and Mexican-Central American Boldoeae are successively sister taxa to the remainder of the family, positions that have moderate to strong support. Within the remainder of the family a North American xerophytic clade has very strong support. Here Bougainvilleae and Pisonieae (and minor additions) form a clade, while Abronieae are embedded in a highly paraphyletic Nyctagineae plus Boerhavieae complex (= Nyctagineae above: Douglas & Manos 2007; see also Levin 2000 for a more limited study).
Classification. For the tribal classification, see Douglas and Spellenberg (2010); they also recognised a monotypic Caribeeae Douglas and Spellenberg, but this was not placed in the phylogeny.
[Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]: fruit a loculicidal capsule [?level].
Evolution. Divergence & Distribution. The stem-group age of this clade is dated to 55-53 m.y.a. (Arakaki et al. 2011).
Edwards and Ogurn (2012) discuss the evolution of CAM and C4 photosynthetic syndromes in this clade.
MOLLUGINACEAE Bartling, nom. cons. Back to Caryophyllales
Barely succulent herbs (shrubs), growth sympodial, modules with definite numbers of leaves; hopane saponins, C-glycosylflavonoids, anthocyanins +; wood rayless; (C4 photosynthesis +); cork?; (secondary growth normal); (sieve tube plastids with starch grains); pericyclic fibres +; (raphides +); (also rhomboidal crystals +); plant glabrous or hairs stellate; cuticle waxes as platelets or rodlets; stomata anomocytic; prophylls prominent; leaves often pseudoverticillate, opposite or spiral, stipules membranaceous (0); P (4) 5, quincuncial, (C bifid to laciniate, -20 [Glinus]); A (2-)5-10(-30), alternate with P, (centrifugal), filaments ± connate basally or not; (pollen polyporate); G (1) [2-5(more)], opposite sepals/perianth or the median member adaxial, placentation axile, style single, or ?styles separate; ovules 1 [basal]-many/carpel, parietal tissue 1(-2) cells across, nucellar cap to 2 cells across, funicles short to long; fruit a loculicidal capsule, or dehiscing by transverse slits, (nut); seeds arillate or not, (operculate); exotestal cells undistinguished in shape; n = 9.
9[list]/87: Mollugo (35), Pharnaceum (20). Largely S. Africa, Glischrothamnus NE Brasil, a few ± tropical to warm temperate, some weedy (map: from Frankenberg & Klaus 1980; Jalas & Suominen 1980; Fl. N. Am. 4: 2003; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011). [Photos - Habit & Flower]
Evolution. Divergence & Distribution. The age of stem group Molluginaceae is estimated at ca 51.9 (± 4.7) or 56.1 (± 5.8) m.y. and crown group diversification started ca 46.7(± 4.8) or 50.3 (± 5.8) m.y.a. (Christin et al. 2011a: estimates depend on age of angiosperms).
The rate of diversification of the Adenogramma-Pharnaceum clade is notably less than many others in this general area of Caryophyllales (Arakaki et al. 2011).
Ecology & Physiology. C4 photosynthesis probably arose more than once here (Christin et al. 2010b, 2011, q.v. for dates). There are also a few C3/C4 intermediates with C2 photosynthesis in Mollugo, and species such as Mollugo verticillata that photosynthesize like this may be some 10-20 m.y. old (Christin et al. 2011a).
Chemistry, Morphology, etc. Anthocyanin presence should be confirmed; pigment type is largely unknown from the group (Brockington et al. 2011). The apparent anomalous occurrence of vascular rays in genera like Macarthuria (M. Endress & Bittrich 1993) is less anomalous when these genera are removed from the family; there has been a similar clarification of apparent variation in sieve tube plastid type... Para- dia- and anisocytic stomata sometimes occur; stomatal type should be checked against the new circumscription of the family. The stipule-like structures need examination.
The androecium may be fasciculate; Adamson (1958a) noted that the 20-30 stamens of Hypertelis spergulacea, which belongs here, are in groups.
Some information is taken from Payne (1933, 1935: Mollugo), Adamson (1960: general), Sharma (1963: floral morphology, includes segregates), Hegnauer (1964, 1989, as Aizoaceae: chemistry), Narayana and Lodha (1972: embryology), Behnke (1976) and Behnke et al. (1983a: both sieve tube plastids), Bogle (1970: general), Hofmann (1973: flower, growth), Richardson (1981: flavonoids, but c.f. Behnke et al. 1983b), M. Endress and Bittrich (1993: general), Bhargava (1934), Narayana (1962a) and Hassan et al. (2005a: seeds and ovules) and Vincken et al. (2007: saponins).
Phylogeny. Mollugo and relatives and Pharnaceum and relatives each formed a well-supported clade, but the two were only weakly linked (Nepokroeff et al. 2002). However, support for a monophyletic Molluginaceae was strong both in Christin et al. (2011a) and Arakaki et al. (2011), and resolution of relationships within the clade was also good; branches in the Adenogramma-Pharnaceum clade were notably long (Arakaki et al. 2011).
Mollugo is strongly para/polyphyletic (Christin et al. 2010b, 2011a; Arakaki et al. 2011).
Classification. The limits of the family have long been unclear. Most Molluginaceae as circumscribed in M. Endress and Bittrich (1993) are included here, but Limeum and relatives Limeaceae), Corbichonia (Lophiocarpaceae), and Macarthuria, are elsewhere in the core Caryophyllales. Polpoda is not incorporated in any description. It has P 4, A alternating with the perianth, G , basally connate styles, and scarious stipules (Hoffman 1994). There have been suggestions that Gisekia might be included in Phytolaccaceae-Rivinioideae (see Cuénoud et al. 2002), although here it is in its own family (Brockington et al. 2009).
Synonymy: Adenogrammaceae Nakai, Glinaceae Martius, Pharnaceaceae Martynov, Polpodaceae Nakai
[Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]] / Portulacinae / Cactinae: (plants with tuberous roots [at least some species in all families]); (CAM +); phloem parenchyma cells with phytoferritin [crystalline iron-protein complex in plastids]; Ca oxalate crystals in stem epidermis; mucilage cells +; stomata paracytic; leaves ± succulent, amphistomatic [?Basellaceae]; two pairs of bracteoles, inner pair in the median plane, lacking subtending buds, ± enclosing the flower; P petal-like, median P abaxial; pollen pantocolpate; style +, branches spreading; ovule lacking funicular/placental obturator; 6-bp deletion in ndhf gene.
Evolution. Divergence & Distribution. Estimates of ages for the crown group (as Cactinae) are (33.7-)18.8(-6.7) m.y., not very old (Ocampo & Columbus 2010: 95% highest posterior density - there see also several other ages for clades in this group); it seems to be New World in origin.
Ecology & Physiology. Ocampo and Columbus (2010) discuss the evolution of various photosynthetic pathways in this clade, which they reconstruct as being plesiomorphically C3. For CAM in Portulacaceae s. l., i.e., scattered through this clade, see Guralnick and Jackson (2001) and especially Ocampo and Columbus (2010). CAM cycling is common; this occurs when plants do not completely shut their stomata during the day, and carbon is fixed at night not from atmospheric but from respiratory CO2.
For estimates of the numbers of succulent species in the various families, see Nyffeler and Eggli (2010b). Taxa with fleshy roots are scattered throughout the clade, being found in all families (except the monotypic Halophytaceae) as well as in all subfamilies of Cactaceae (e.g. Nyffeler et al. 2008).
Chemistry, Morphology, etc. Variation within this clade is complex (see also Nyffeler 2007, especially Ogburn 2007; Nyffeler et al. 2008; Ogburn & Edwards 2009; Nyffeler & Eggli 2010; Ocampo & Columbus 2010). Most taxa have mucilage cells, but there may be interesting variation within the group as to exactly where such cells occur in the plant (Ogburn & Edwards 2009).
Interpretation of the parts surrounding the flowers is complicated by the terms that have been used to describe them in the past. Often there are paired structures borne immediately below the flower and more or less completely surrounding it. These are called bracteoles here, but they have often been called sepals. The whorl inside the bracteoles, usually 4- or 5-parted, is called a perianth, and is like that of other core Caryophyllales. Its members are often more or less brightly coloured and have been called petals or petal-likes. Flowers often have more than a single pair of bracteoles. The inner/upper pair of bracteoles is in the median plane (e.g. Eichler 1878), as is the sole pair of bracteoles in Montia (Ronse de Craene 2010) and Halophyton (Pozner & Cocucci 2006), although they do not comment on this. The transverse bracteoles may have flowers in their axils, the inner median bracteoles always lack them. In at least some species of Anacampseros the upper bracteoles are in the same plane as the bud-subtending bracteoles (Vanvinckenroye & Smets 1999), while in species of Portulaca such as P. oligosperma there are two quite large bracteoles immediately underneath the flower and then four smaller bracteoles in a whorl separated from the first pair by a short internode (Geesink 1969).
Portulaca has an androecial ring primordium, as in some Cactaceae and in species of Anacampseros, sometimes also with centrifugal initiation of stamens; other species have fewer stamens, which may be initiated in pairs (facing each other!) opposite the perianth members, or as single stamens alternating with them (Vanvinckenroye & Smets 1999). When there is the same number of stamens as perianth members, their positions relative to the carpels varies. Nowicke (1996) summarized a number of pollen characters that are shared in the group (her Portulacinae), although they might also occur outside it: Columellae either narrowed towards the middle or expanded towards the base, sometimes fused; pollen with granular internal surfaces; perforated foot layer; non-apertural endexine "thread-like" - the latter term unclear from the descriptions provided.
For chemistry, see Hegnauer (1969, 1990), for floral diagrams, see Ronse de Craene (2010). For anatomical information about the old Portulacaceae, see Becker (1895), for pollen, see Nilsson (1967), for general information, see Carolin (1987 [also a phylogenetic analysis], 1993). For information on the vegetative plant, see Nyffeler et al. (2008).
Phylogeny. Relationships between members of this clade were for some time rather uncertain, but it was clear that they were not reflected by the then-current classifications. Hershkovitz and Zimmer (1997) realized that if Cactaceae were recognised, Portulacaceae would be paraphyletic (see also Appelquist & Wallace 1999, 2001). Later they found little major phylogenetic structure in a study of American Portulacaceae, yet there must have been a number of major dispersal/colonization events in the group (Hershkovitz & Zimmer 2000: ribosomal DNA, Cactaceae not included). Hershkovitz (2006) found the same general pattern as he focused on W. American "Portulacaceae" from the Andean region - there were perhaps half a dozen clades in that region, but no major groupings beyond that. Cactaceae, Didiereaceae and Portulacaceae remained a closely entwined complex (Appelquist & Wallace 2000). Indeed, they can all be intergrafted (Anderson 1997). See also Cuénoud et al. (2002) for relationships in this area, e.g. of Halophytum.
A number of studies since 2007 have clarified relationships further. Cactaceae + Talinum + Portulaca + Anacampseros, etc., were found to make a major and rather well supported clade (Hershkovitz & Zimmer 1997; Appelquist & Wallace 2001). Nyffeler (2007: three genes, two compartments) found some support for a topology [Talinum and relatives [Portulaca [Anacampseros and relatives + Cactaceae]]], although the topology was different when the mitochondrial nad1 data were analyzed alone. Support for the [Anacampseros and relatives + Cactaceae] clade was appreciable in the combined analysis (78% bootstrap), where the chloroplast signal predominated. Details of relationships around Cactaceae remained unstable. Brockington et al. (2009; large amounts of data, rather skimpy sampling) found a clade [Portulacaceae + Talinaceae] with 98% boostrap support, and Claytonia sister to the whole clade, including Halophytaceae; Nyffeler and Eggli (2010) found few resolved relationships except in the Talinaceae-Cactaceae area, and support for the monophyly of Didieraceae and Montiaceae was not strong; and Butterworth and Edwards (2008) found the relationships [Anacampserotaceae [Talinacaeae [(weak support)Portulacaceae + Cactaceae]]], although there was no outgroup, so Anacampserotaceae appeared to be paraphyletic. Many of the relationships found by Ocampo and Columbus (2010) were also poorly supported, and Halophytaceae were wandering around the tree, while Soltis et al. (2011) found Molluginaceae to be sister to the rest of the group, although support was only moderate.
Most recently, a two-pronged study by Arakaki et al. (2010) has thrown considerable light on relationships. An analysis of a number of chloroplast genomes confirmed the general position of Caryophyllales (see the Dilleniales page for more discussion). Using the nuclear PHYC and chloroplast trnK/matK genes and ca 250 species of this clade, Arakaki et al. (2011) confirmed with strong support the position of Molluginaceae as the sister taxon of this clade. There was strong support for relationships along the spine of this clade, but "only" 78% likelihood bootstrap support for the [Anacampserotaceae [Portulacaceae + Cactaceae]] clade, although that also has some morphological support. Support for the monophyly of all families is strong. The only exception is the [Halophytaceae [Didiereaceae + Basellaceae]] clade; Didieraceae are not monophyletic, Basellaceae being sister to the Portulacaria group, and Halophytaceae are only weakly associated with the other two families (Arakaki et al. 2011).
Classification. Basellaceae and Didiereaceae do remain distinct, although a few African genera of Portulacaceae have been placed with the latter; morphology is largely consistent with their new positions. Portulacaceae are strongly paraphyletic, and erstwhile members occupy several pectinations on the clade immediately basal to Cactaceae, while within Cactaceae the "basal" Pereskia has turned out to be paraphyletic. The Antipodean Hectorellaceae have often been placed around here, but Halophytaceae were not considered part of this group.
For family limits and characterisations, see Nyffeler and Eggli (2010).
MONTIACEAE Rafinesque Back to Caryophyllales
Annual to perennial herbs, often with swollen roots and basal rosette leaves, internodes short (subshrubs; leaves not succulent - Montiopsis, etc.); photosynthesis?; cork cambium initiation delayed; secondary growth little; vessel elements?; nodes 1:1 [Lyallia]; plant glabrous; stomata longitudinally oriented; cuticle waxes as procumbent platelets; leaves often with broad clasping bases, flat, to terete with an adaxial impressed line; inflorescences terminal or axillary, (monochasial) cymose, or single (axillary) flower; (transverse bracteoles absent); P 4-5(-19), (basally connate); A equal and opposite perianth members, (or 1 fewer, alternating with P - Hectorella, Lyallia; -100, development centrifugal), basally connate or not; pollen also 3-colpate, pantoporate; G [2-8], (placentation free central, with 4-7 ovules), style ± developed, branches diverging; ovules with parietal tissue ca 5 cells across, in radial rows, funicle?; fruit also circumscissile, or 1-seeded, indehiscent; outer wall of exotesta thickened and with stalactite-like projections; n = 6-13, etc.
ca 10/: Parakeelya (40-50), Claytonia (27). Especially Western North and South America, also the Antilles and the Subantarctic Islands (map: approximate, from Hultén & Fries 1986; Fl. N. Am. 4: 2003; Miller & Chambers 2006; M. Ogburn, pers. comm. ix.2012; Australia's Virtual Herbarium i.2013 - much naturalization, so not easy). [Photo - Collection, but not all.]
Evolution. Divergence & Distribution. The age for crown-group Montiaceae is (25.4-)13(-3.4) m.y. (Ocampo & Columbus 2010: 95% highest posterior density).
Ecology & Physiology. Within this clade, Montiaceae are noted for their ecological expansion into both colder and more seasonally variable habitats, and there have been several habit/habitat shifts within the clade (Ogburn & Edwards 2012).
Pollination Biology & Seed Dispersal. The seeds may be forcibly ejected as the margins of the valves incurve during capsule dehiscence (Carolin 1993). The seeds of some Montiaceae are myrmecophytic (Lengyel et al. 2010).
Bacterial/Fungal Associations. The South American Calandrinia is a host of the anther smut Microbotryum (Uredinomycota), also found on Silene, etc. (Hood et al. 2010).
Chemistry, Morphology, etc. Hectorella has both spiral phyllotaxis and a closed vascular system, a very unusual combination (Beck et al. 1982). The inflorescence of Hectorella and Lyallia may be a reduced cyme; there are alternate/distichous bracts below the flower, and the latter genus may have more than one flower per axil (Skipworth 1961; Wagstaff & Hennion 2007). The paired bracteoles below the flower in these two genera are clearly described and illustrated as being transverse (lateral) by Skipworth (1961), but later described as being ad/abaxial (median) by Philipson and Skipworth (1961).
Cave et al. (2010) described the lower two bracteoles of Calandrinia as developing successively, the upper pair being lateral(-abaxial). Montiopsis can have trilobed bracteoles. Nyffeler and Eggli (2010) describe the flower as having up to 9 "sepaloids" (= perianth members) in Lewisia. Schnizlein (1843-1870: fam. 206) showed carpels alternating with the perianth members, or the median member in the abaxial position, as in Claytonia. Claytonia virginiana shows extreme variation in chromosome numbers - 2n = 12-ca 191 (Bogle 1969).
Some information is taken from Philipson (1993) and Lourteig (1994); see Meunier (1890) for ovules and seeds, for pollen, see Nilsson (1967); see Carolin (1993) and Nyffeler and Eggli (2009) for general accounts.
Phylogeny. West American members of the old Portulacaceae placed here include Montia, Lewisia, Phemeranthus (this used to be included in Talinum - Talinaceae here), etc. (e.g. Hershkovitz 1993, 2006; Hershkovitz & Zimmer 2000). Applequist et al. (2006: ndhf analysis, see also Nepokroeff et al. 2002) included the New Zealand-Antarctic Hectorellaceae, previously of uncertain relationships, here (as a new tribe of Portulacaceae). The whole clade has strong support, as does the sister group relationship between Phemeranthus and the nine other genera included ((Applequist et al. 2006). Although flower position (axillary) and bracteole and stamen position of Hectorellaceae differ from that of Montiaceae, and the gynoecium is unilocular, the anatomy of the two is very similar (Carlquist 1998b).
O'Quinn and Hufford (2005) outlined the phylogeny of Claytonia (tricolpate pollen) and its sister taxon, Montia (pantocolpate).
Synonymy: Hectorellaceae Philipson & Skipworth
[[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]: ?
[Halophytaceae [Didiereaceae + Basellaceae]]: ovary with single basal ovule; fruit indehiscent, single-seeded.
HALOPHYTACEAE A. Soriano Back to Caryophyllales
Annual herb; successive cambia +; wood rayless; stomata?; plant monoecious, pedicels 0; nectary 0; staminate inflorescence: densely spicate; transverse bracteoles absent; P 4, barely petal-like, valvate-decussate; stamens alternate with perianth members, anthers extrorse, dehiscing by pores by contraction of the connective, endothecium with frame-shaped thickening on anticlinal walls; pollen cuboid, hexaporate; pistillode 0; carpellate inflorescence: fasciculate; P 0; staminodes 0; G , unilocular, [adaxial carpel fertile], style +, stigmas spreading; fruit a nutlet, several becoming embedded in hard inflorescence axis; n = 12.
1[list]/1: Halophytum ameghinoi. Argentina (map: from Zuloaga & Morrone 1999).
Chemistry, Morphology, etc. There are no endothecial thickenings at all on cells adjacent to the openings of the anthers (Pozner & Cocucci 2006).
Some information is taken from Bittrich (1993b: general); Pozner and Cocucci (2006) describe the staminate flower in considerable detail, including the distinctive endothecial thickenings and anther dehiscence.
Previous Relationships. Halophytaceae were included in Chenopodiaceae (Cronquist 1981). Relationships with Aizoaceae - also with rayless wood - have been suggested (Gibson 1978).
[Didiereaceae + Basellaceae]: ?
Evolution. Divergence & Distribution. The age for this clade is (28.5-)14.9(-3.9) m.y. (Ocampo & Columbus 2010: 95% highest posterior density).
Phylogeny. There is weak support for this family pair in Soltis et al. (2011).
DIDIEREACEAE Radlkofer, nom. cons. Back to Caryophyllales
Woody, ± stem succulents, often thorny, (deciduous; short shoots +); CAM or facultative CAM; "tannin" common, methylated flavonoids +; (wide-band tracheids +); cork cambium initiation precocious; tanniniferous cells +; leaf stomata parallelocytic, transversely oriented; cuticular waxes as ribbons or rodlets; short shoots common, (persistent paired prophylls); plant (gyno)dioecious, (inflorescence fasciculate); (transverse bracteoles absent); P 4-5, annular nectary at base; A 5 [alternating with P]-12 in a single whorl (many - Calyptrotheca), from ring primordium, basally connate, (with adaxial nectaries); pollen tricolpate, 5-7-zonocolpate (polyporate), aperture finely spinate; G [(2-4)], stigmas ± peltate, fringed; ovules 1(-2)/carpel; fruit achenial, (circumscissile capsule, K strongly accrescent - Calyptrotheca); seeds with funicular strophiole or aril; perisperm ± absent; n = 22, 24, often wildly polyploid.
7/16. Madagascar, South Africa, E. Africa (Map: from Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photos - Collection.]
Evolution. Divergence & Distribution. The age for crown-group Didiereaceae is (24.4-)12.1(-2.4) m.y. (Ocampo & Columbus 2010: 95% highest posterior density).
Chemistry, Morphology, etc. Rauh (1983) calls the spiky structures of Didiereaceae s. str. spines, being either leaves on short shoots or paired and stipular. However, Alluaudia has leaves subtending an axillary spiky structure, and later paired and apparently prophyllar leaves develop from an axillary bud below it. This suggests that the spiky structure is a modified axillary shoot, a thorn.
The bracteoles immediately associated with each flower are in the median plane, and large bracteoles of the inflorescence ("large bracts") may be obvious, as in Portulacaria. In Didiereaceae s. str. there are four stamens clearly alternating with the perianth members.
See Rauh and Schölz (1965: growth, morphology, etc), Hegnauer (1966, 1968, 1989: chemistry), Kubitzki (1993b: general), Schatz (2001: generic descriptions), Erbar and Leins (2006: floral ontogeny), and Nyffeler and Eggli (2009: general).
Phylogeny. This clade includes a morphologically distinctive monophyletic group of plants that are Didiereaceae in the old sense. Immediately basal to them are some African ex-Portulacaceae - [[Ceraria (Africa; looks like Didiereaceae s. str.!) + Portulacaria (both with tricolpate pollen)] [Calyptrotheca (polyporate) + Didiereaceae (in the old sense)]]. Didiereaceae should be expanded to include the whole clade (Appelquist & Wallace 2000, 2003). Appelquist and Wallace (2003) provide a subfamilial classification for the expanded Didiereaceae.
Synonmy: Portulacariaceae Doweld
BASELLACEAE Rafinesque, nom. cons. Back to Caryophyllales
Vines/lianes, with swollen rhizomes or tubers; successive cambia +; cork cambium initiation timing?, in outer cortex; vascular bundles separate, bicollateral; leaf stomata paracytic, ?oriented; cuticle wax crystalloids 0; (leaves also opposite), (lamina vernation conduplicate [Anredera]), (margins serrate, with glands - Tournonia); inflorescence racemose, (cymose - Tournonia); flowers small; P (4-)5(-13), ± connate; A 4-9, often equal and opposite perianth members, adnate to them, basally connate, tapetal cells multi-nucleate; pollen hexacolpate/porate (cuboid); (style single, branches short), stigma ± capitate or lobed; ovule single, basal, outer integument ca 2 cells across, inner integument 2-4 cells across, parietal tissue ca 8(?-16) cells across, nucellar beak +, no space between the integuments, funicle shortish; fruit an utricle, surrounded by persistent (bracteoles and) P, (P fleshy); testa in particular multiplicative, also tegmen; perisperm scanty, starch grains clustered, embryo green; n = 12, 22.
4[list]/19. Africa, New World, apparently introduced into India-East Asia (map: from Sperling 1987; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. 4: 2003). [Photos - Collection]
Evolution. Divergence & Distribution. The age for this clade is (9-)3.8(-0.4) m.y. (Ocampo & Columbus 2010: 95% highest posterior density, but c.f. sampling).
Chemistry, Morphology, etc. Sperling (1987) reports both bracteoles and large, paired structures immediately surrounding the perianth (see also Eriksson 2007). The interpretation of floral morphology differs - c.f. Friedrich (1956), LaCroix and Sattler (1988) and Sperling and Bittrich (1993).
For general information, see Bogle (1969), Sperling (1987), Eriksson (2007), and Nyffeler and Eggli (2009). For chemistry, see Hegnauer (1964, 1989), for wood anatomy, see Carlquist (1999), for successive cambia, see Jansen et al. (2000c).
Taxonomy. Eriksson (2007) includes a synopsis of species included in the family.
Synonymy: Anrederaceae J. Agardh, Ullucaceae Nakai
[Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]: plant mucilaginous; secondary growth normal; pericyclic fibres 0; stomata parallelocytic; fruit covered by dried P, pericarp 2-layered, exocarp ± caducous.
Chemistry, Morphology, etc. Ex-Portulacaceae in the pectinations basal to Cactaceae have the pericarp strongly differentiated into two layers, they often have hairs and bristles in their leaf axils, and even semi-inferior ovaries.
For anatomy, see Ogburn (2007) and Ogburn and Edwards (2009).
TALINACEAE Doweld Back to Caryophyllales
Herbs to (lianescent) shrubs, underground parts often tuberous; cork cambium initiation timing variable, (cortical); tanniniferous cells +; C3/CAM cycling; petiole bundle arcuate, with wing bundles; stem stomata parallel to stem axis, leaf stomata un- or weakly transversely oriented, morphology variable; P quincuncial; A ca 15, anther wall development monocotyledonous; archesporial cells uniseriate; G , ovary at least initially septate; ovules with parietal tissue 1-2 cells across, nucellar cap to 4 cells across, epidermal cells radially elongate; fruit (baccate, mucilaginous, indehiscent - Talinella), epidermis papillate; seed strophiolate [= funicle?], exotesta well developed, endotegmen thickening slight; n = 8.
?2/27. America and Africa, including Madagascar (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Collection, but not all.]
Evolution. Divergence & Distribution. The age for crown-group Talinaceae is estimated at (18.3-)9.1(-2) m.y. (Ocampo & Columbus 2010: 95% highest posterior density).
Chemistry, Morphology, etc. The roots are apparently polyarch (von Poellnitz 1934). Young leaves may have paired, axillary scales; these are the very tips of the prophylls.
See Meunier (1890: ovules and seeds), von Poellnitz (1934: general), Maheshwari Devi and Pulliah (1975: embryology), Vanvinckenroye and Smets (1996: floral development) and Veselova et al. (2012: embryology); Nyffeler and Eggli (2009) for general information.
Phylogeny. Talinella is nested within Talinum (Nyffeler 2007; Nyffeler & Eggli 2010).
[Anacampserotaceae [Portulacaceae + Cactaceae]]: (sclereids in stem cortex); leaves with axillary bi- or multiseriate hairs/scales +; A many.
Evolution. Divergence & Distribution. The age for this clade is some (26.6-)14.3(-5.1) m.y. (Ocampo & Columbus 2010: 95% highest posterior density, note topology).
Chemistry, Morphology, etc. The axillary hairs found in many of these ex-Portulacaceae are bi- or oligoseriate, while those of the few Cactaceae examined - but from three subfamilies - are uniseriate, although those of Pereskiopsis are biseriate at the base. Chorinsky (1931) remains a useful early study on these structures, which are never vascularized (see also Rutishauser 1981). There is variation in the chloroplast infA gene in this clade, with both insertions and duplications occuring (Ocampo 2009).
ANACAMPSEROTACEAE Eggli & Nyffeler Back to Caryophyllales
Subshrubs with ± tuberous roots, (stems fleshy), (rosette plants), internodes short; cork cambium initiation precocious, (cortical); (wood rayless); (wide-band tracheids +); (sclereids +); facultative CAM, ?C4 photosynthesis; leaf stomata transversely oriented; leaves (opposite), ± terete, (axillary hairs 0, but then concave adaxial scale - Avonia); upper and lower bracteoles in same plane; (A 5-many), basally connate; G [(2) 3], stigmas receptive on both surfaces; (exocarp and endocarp not separating - Grahamia); seeds pale-coloured, (winged), exotesta ± separate from endotesta, thin walled, unlignified, (cells bullate to long-papillate); embryo only slightly (much) curved, not surrounding the poorly developed perisperm; n = 9.
3/32: Anacampseros (30). Very scattered: C. and S. Australia, Somalia to South Africa (most species), S. South America, N. Mexico and S.W. U.S.A. (map: from Gerbaulet 1992a, 1993; Fl. N. Am. 4: 2003).
Evolution. Divergence & Distribution. The age for crown-group Anacampserotaceae is (22.6-)11.4(-3.2) m.y. (Ocampo & Columbus 2010: 95% highest posterior density). For the biogeography of this widely scattered clade, see Gerbaulet (1992b).
Ecology & Physiology. For the ecology of African Anacampserotaceae, see Gerbaulet (1993).
Chemistry, Morphology, etc. For general information, see von Poellnitz (1933: general), Gerbaulet (1992a), Rowley (1994), and Nyffeler and Eggli (2009); for anatomy, etc., see von Poellnitz (1933) and for floral development, see Vanvickenroye and Smets (1999).
Phylogeny. Nyffeler (1997) included six species of Grahamia in his study, and they formed a perfect basal pectination; at least some of the nodes had good support. This helps in reconstructing the basal character states for the clade - whatever characters Grahamia has, those are the characters of the family as a whole...
Classification. For genera, see Nyffeler and Eggli (2009).
[Portulacaceae + Cactaceae]: unlignified parenchyma cells in wood; G half inferior; pericarp not 2-layered.
Chemistry, Morphology, etc. Non-lignified parenchyma cells, often in bands, occur in the wood of at least some Portulaca and in Cactaceae (Melo-de-Pinna 2009). Portulaca and Pereskia (but not Claytonia) share a 500 bp chloroplast DNA deletion in the rbcL gene (Wallace & Gibson 2002 for details and references), a potentially informative molecular marker.
PORTULACACEAE Jussieu, nom. cons. Back to Caryophyllales
Succulent (annual) herbs, (roots tuberous); cork cambium initiation delayed; (wood rayless); C4 photosynthesis/CAM cycling; leaf stomata transversely oriented; (internodes short); leaves ± terete, (axillary hairs 0); inflorescences terminal, ± capitate, with involucre; (transverse bracteoles absent); (P 4-8), (connate), with a single trace; tapetal cells multi-nucleate; G [(4-)5(-8)]; ovules with parietal tissue ca 5 cells across, in radial rows, or ca 8 cells across, not in rows [P. pilosa]; capsule circumscissile; seed with hilar aril; anticlinal walls of testa sinuous; n = (8-)10, x = 9.
1/40-100. Worldwide, but especially tropical and subtropical North and South America, weedy (map: approximate, from Legrand 1962; Geesink 1969; Frankenberg & Klaus 1980; Gilbert & Phillips 2000; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase ii.2010). [Photo - Collection, but not all.]
Evolution. Divergence & Distribution. Ages suggested for crown-group Portulaca are (18.5-)9.6(-2.0) m.y. (Ocampo & Columbus 2010: 95% highest posterior density) and (43-)23(-6.9) m.y. (Ocampo & Columbus 2012: improved sampling, calibration on Hawaiian islands).
Chemistry, Morphology, etc. See Meunier (1890) for ovules and seeds, Sharma (1954) for floral anatomy (the single traces to the P members divide into three), and Nyffeler and Eggli (2009) for general information.
Ecology & Physiology. There have been several switches to C4 photosynthesis at a maximum ca (33.8-)28.8(-23.8) m.y.a. (Ocampo & Columbus 2009) and at a minimum about 1/3 this (Christin et al. 2011b: s.d.).
Phylogeny. For relationships within Portulaca, see Ocampo and Columbus (2009); taxa with opposite leaves and those with spiral leaves form separate clades.
Previous Relationships. For taxa included in earlier circumscriptions of Portulacaceae, see Carolin (1993) and Nyffeler and Eggli (2009).
CACTACEAE Jussieu, nom. cons. Back to Caryophyllales
± Woody; C3/CAM cycling; rays wide and tall; calcium oxalate as whewellite [CaC2O4.H2O]; cork cambium initiation precocious; extensive primary expansion of the pith; (sclereids in phloem); nodes often with two or many traces; epidermis (inc. cuticle) thick-walled, hypodermis +, druses + (0), numerous; leaf stomata unoriented; cuticular waxes as ribbons or rodlets, also thick prostrate plates; short shoots [areoles] with spines [= leaves], photosynthetic leaves, and uni- or biseriate hairs, (areoles long-lived, spines continuing to be produced); long shoot leaves fleshy; (inflorescence proliferation); median bracteoles 0; P several-numerous, spiral, outer sepaline and inner petaline [modified ?bracts]; A centrifugal, initially from five separate primordia; nectary rather disc-like; G [5-many], surrounded by stem tissue [with areoles, etc.]; placentation ± parietal, stigma wet; ovules many/carpel, outer integument ca 2 cells across, inner integument 2(-3) cells across, parietal tissue ca 1 cell across, nucellar cap +, nucellar epidermal cells radially elongated, lateral epidermal cells anticlinally divided [?all], funicle with short hairs apically (not), long; fruit baccate; funicles fleshy; endotegmic cell walls thickened or not; x = 11; 6 kb inversion in large single copy region of plastid genome.
131[list]/1866 - five groups below. Nearly all New World, esp. arid conditions, perhaps a few also Old World. [Photos - Collection.]
1. Northern, Caribbean Pereskia, = Rhodocactus
Cork cambium initiation precocious, cortical; no stem stomata; (P laciniate); pollen colpate; (G inferior).
1/7. Mexico and the Caribbean, Brasil. (map: from Leuenberger 1986, 2008; Edwards et al. 2005)[Photo - Leaf, Flower, Fruit.]
[Pereskioideae [Opuntioideae [Maihuenioideae + Cactoideae]]] / caulocacti: cork cambium initiation delayed; cortical sclereids 0; stem mucilage cells +; stem epidermis persistent, cuticle often thick, stomata +, parallely oriented, opuntioid [apart from the innermost pair of cells, subsidiary cells distinct, but more or less randomly arranged].
2. Pereskioideae Engelmann
(Tuberous roots); phloem sclereids +; lamina supervolute; A centrifugal, from 5 primordia; pollen polycolpate.
1/9. Andean, S. South America, = Pereskia s. str. (map: from Leuenberger 1986, 2008; Edwards et al. 2005).
[Opuntioideae [Maihuenioideae + Cactoideae]]: CAM or facultative CAM +; stems succulent; extensive primary expansion of the cortex[?]; internodes short; wide-band tracheids in secondary xylem [at least in seedlings]; subepidermal collenchyma +; cortical chlorenchyma forming mesophyllar tissue with intercellular spaces; epidermis persistent; areoles not producing leaves [other than spines]; leaves terete; inflorescences axillary [in areoles], flowers solitary; A from ring primordium; stigma commissural [?Maihuenoideae]; G inferior.
3. Opuntioideae Burnett
Plant ± shrubby; stems terete, usu. articulated, often flattened; calcium oxalate hypodermal, as druses or spherical clusters; roots often tuberous; (cork cambium initiation precocious); (no stem stomata); leaf stomata parallely oriented; leaves small, terete, soon deciduous, (subpersistent, large, with blade - Pereskiopsis); areoles with minute, retrorsely-barbed bristle-spines [glochids]; (hypanthium +, short); pollen polyporate; seeds ± covered by bony funicule ["aril"], outer periclinal wall of testa little thickened; (cotyledons are storage organs of seed); deletion of the chloroplast accD gene.
16/349: Opuntia (200). Canada, almost the Arctic Circle, to Patagonia. (map: see Thorne 1973; F. N. Am. vol. 4. 2003.) [Photo - Flower, Flower.]
Synonymy: Nopaleaceae Schmid & Curtman, Opuntiaceae Desvaux
[Maihuenioideae + Cactoideae]: inflorescence not proliferating; testa interstitially pitted or cratered, exotesta with outer periclinal wall much thickened.
4. Maihuenioideae P. Fearn
Plant densely caespitose\; cork cambium initiation precocious; large mucilage reservoirs in stem medulla and cortex; photosynthetic parenchyma at base of areolar crypts, no stem stomata; leaf stomata transversely oriented; (areoles producing leaves), leaves terete, deciduous, with cylindrical reticulum of bundles, the external xylem surrounding central mucilage reservoir; pollen tricolpate; funicles in fruit long, mucilaginous.
1/2. Argentina and Chile (map: from Leuenberger 1997, 2008).
5. Cactoideae Eaton
(Stem dichotomising); (roots tuberous); plant essentially leafless [leaves up to 1.5(-2.5) mm long when mature]; calcium oxalate also as weddellite [CaC2O4.2H2O]; stem stomata unoriented [transverse - epiphytic taxa]; pollen 3-polycolpate(-porate), (in tetrads); (outer integument 3-4 cells across - Cereus), funicles?; seeds with a conspicuous spongy hilum-micropyle region; loss of intron in the chloroplast rpoC1 gene.
112/1498. New World, S. Canada to S. W. U.S.A. southwards; perhaps few in Africa, Madagascar, and Sri Lanka - only Rhipsalis.
5A. Blossfeldieae Crozier
Spines absent; vascular bundles lacking cap of phloem fibres; subepidermal collenchyma 0; epidermis (inc. cuticle) thin-walled, soon replaced by cork cambium, hypodermis 0; photosynthetic parenchyma at base of areolar crypts; stem stomata few, in areolar crypts, leaf stomata 0; seeds with a funicular aril [strophiolate]; testa with one short narrow hair per cell.
1/2. Bolivia to Argentina, eastern Andes (map: from Leuenberger 2008).
5B. Cacteae Reichenbach / The Rest.
(Plant epiphytic [ca 1/10 spp.]; climbers); stem ribbed and/or tuberculate (not); (growth determinate); calcium oxalate usually as weddellite (and/or whewellite), (raphides +); (alkaloids +); (wide-band tracheids 0); cortical vascular bundles +; cortex broad, succulent, (inner cortical cells collapsible); (areoles dimorphic); (flowers monosymmetric); hypanthium + (0); pollen 3-polycolpate(-porate); (ovules circinotropous); (seeds arillate), funicles?; (hypocotyl storage organ); rpoC1 intron lost.
91/1250: Mammillaria (145-180), Echinopsis (50-100), Echinocereus (50), Gymnocalycium (50), Rhipsalis (40). New World (S. Canada to S. W. U.S.A. southwards), esp. Mexico, Brasil, Peru-Bolivia; Rhipsalis with a few spp. in Africa, Madagascar, Sri Lanka; also rain forest climbers and epiphytes (map: see Thorne 1973; Barthlott 1983 and Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003 [Rhipsalis]; Fl. N. Am. vol. 4. 2003.). [Photo - Plant, Flower.]
Synonymy: Cereaceae de Candolle & Sprengel
Evolution. Divergence & Distribution. Diversification in Cactaceae is estimated to have occurred in the mid-Tertiary ca 30 m.y.a. (Hershkovitz & Zimmer 1997, q.v. for other estimates), so [Opuntioideae [Maihuenioideae + Cactoideae]] may be a rather young group. Ocampo and Columbus (2010: 95% highest posterior density) suggest still younger ages of ca 14 or (19.1-)10(-3.1) m.y. for stem and crown group Cactaceae. However, Arakaki et al. (2011) suggest an age of around 35 m.y. for stem Cactaceae, and ca 28 m.y. for crown diversification, diversification in core cacti, the [Opuntioideae [Maihuenioideae + Cactoideae]] clade, occuring somewhere between 27 and 25 m.y.a.. See also Nyffeler and Eggli (2010a) for some dates.
Arakaki et al. (2011) note a number of clade ages and diversification rates within Cactaceae, and many of the latter are quite high, with significant radiations occuring in the late Miocene-Pliocene, ca 8-3 m.y.a. The Pachycereae, which include the North American columnar cacti, also began diversifying about then (ca 8.5 m.y.a.: Barba Montoya et al. 2011). However, the monotypic Blossfeldia, sister to all other Cactoidaeae (see below), shows notably lowered diversification rates of 0 or 2.27 x 10-17/ma, depending on the particular measure used (Arakaki et al. 2011). Crown group Opuntia in the narrow sense, with 150-180 species, may be (7.5-)5.6(-3.6) m.y. old (Araki et al. 2011). Originating in southwest South America, it may have moved to North America by long-distance dispersal, and it subsequently diversified there considerably (Majure et al. 2012).
Cactaceae are an iconic family of the New World, but Rhipsalis, epiphytic and bird-dispersed, has a few species growing in Africa, Madagascar, and Sri Lanka; there have been questions as to whether the Old World species are native, or not (Barthlott 1983).
As Edwards et al. (2005) note, the anatomy of the outgroups to Cactaceae is unfortunately poorly known, as is the occurrence of proliferating inflorescences in Portulaca, with a more or less inferior ovary and now thought to be sister to Cactaceae (c.f. Edwards et al. 2005).
Plant/Animal Interactions. The cactus-feeding habit may have evolved only once in the pyralid phycitine moths, although support is weak (Simonsen 2008: morphology only). This group includes the famous/infamous (it depends on where you live) Cactoblastis cactorum. The Drosera repleta species group has radiated on Cactaceae, the young growing on fermenting cactus tissues, whether cactus pads or the stems of columnar cacti (Oliveira et al. 2012); they moved on to this habitat from fermenting fruits perhaps 16-12 m.y.a. Some Drosophila will grow on only a single host, the latter containing sterols that can stand in for essential sterols missing from the ecdysone pathway of the insect (Lang et al. 2012).
Ecology & Physiology. Edwards and Donoghue (2006; see also Edwards 2006; Edwards & Diaz 2006; Ogburn & Edwards 2010) discuss the eco-physiological evolution of Cactaceae (for which, also see Nobel 1988 and references). They emphasize that the leafy Pereskia and Rhodocactus clades have high photosynthetic water use efficiency, very high minimum leaf water potentials, and conservative stomatal behaviour, the stomata opening only when there is available water, at night or after rain. Other features of potential functional interest include the production of large amounts of water conducting tissue relative to leaf area, and perhaps also CAM-type photosynthesis. This latter is poorly developed in Pereskia, etc., but is well developed in succulent cacti (Martin & Wallace 2000).
Most Cactaceae have a broad, shallow rooting system that allows quick uptake of water after rain. In some Cactoideae, at least, the primary root is determinate in growth, perhaps facilitating the rapid development of lateral roots (Rodríguez-Rodríguez et al. 2003). "Rain roots", water-absorbing roots, develop quickly after rains and die when the soil dries up. Here, too, the apical root usually aborts (Shishkova et al. 2008; Ogburn & Edwards 2010), but a skeletal root system of perennial, cork-covered roots persists (Gibson & Nobel 1986). Contraction of the roots, so keeping the plant close to the ground surface, is known or suspected for some Cactoideae (Garrett et al. 2010). Roots in at least some Cactaceae have rhizosheaths surrounding and adherent to the root and perhaps protecting it against dessication; they are formed by mucilage from the root, soil grains, etc. (Huang et al. 1993).
Fleshy, water-storing roots are scattered in Cactaceae, including Pereskia (e.g. Rauh 1979); the taxa involved are usually small plants. The tissue involved is not always the same, suggesting the independent origin of such roots, but it is some kind of modified secondary vascular tissue (Stone-Palmquist & Mauseth 2002). These swollen roots seem to be particularly common in the taxa of the basal pectinations of Opuntioideae (Griffith & Porter 2009), and they are also common in families in the pectinations immediately basal to Cactaceae as a whole (see also Griffith 2004).
Diversification of the "leafless" Cactaceae may be as much connected with the development of a cauline water storage system as with the evolution of the other ecophysiological features just mentioned (and of course one would like to know much more about the physiology and anatomy of the clades immediately basal to Cactaceae...). The ribbed and/or tuberculate stems of most Cactoideae may allow the loss and gain of large amounts of water as the stem can easily contract or expand (see also Mauseth 2006a). Few cacti are really dessication tolerant, but Blossfeldia is an exception (Grifith 2009). Finally, although Cactaceae are pre-eminently a group of drier climates in the New World and a notable component of seasonally dry tropical forests (Pennington et al. 2009), a number of taxa grow in more or less humid forest as lianes and epiphytes, several having flattened and leaf-like stems; the epiphytic habit may have evolved four times or so in Cactoideae (Korotkova et al. 2010).
Calcium oxalate metabolism in Cactaceae and relatives is potentially interesting. There is variation in the degree of hydration of calcium oxalate, and the general distribution of the two crystal forms found, weddellite (CaC2O4.2H2O) and whewellite (CaC2O4.H2O), may be systematically interesting (Rivera and Smith 1979: they note only druses were examined; Monje & Baran 2002; esp. Hartl et al. 2007). Some Cactaceae accumulate positively massive amounts of calcium oxalate crystals, for example, they make up ca 85% of the dry weight of Cactus senilis.
On a totally different subject, grafts between taxonomically widely distant taxa are easy to make in Cactaceae. For instance, Blossfeldia can be grafted onto Pereskiopsis, and contamination of Blossfeldia DNA by that of its stock was fingered as a possible cause of early conflicts over the phylogenetic position of that remarkable genus (Gorelick 2004).
Pollination Biology & Seed Dispersal. The evolution of a hypanthium and so the possibility of developing a long floral tube may have been a key innovation for Cactoideae allowing a greater diversity of pollinators for the flowers; Cactoideae are much more speciose than other clades in this phylogenetic area (Schlumpberger 2012). Bee pollination is probably plesiomorphic in Cactaceae; there have been perhaps 10 bee-to-humming bird pollinator shifts and half as many bee-sphingid moth shifts, mostly in Cactoideae (Schlumpberger 2012). A variety of other pollinators visit cacti flowers, and about 200 species in 51 genera are pollinated by bats (Dobat & Peikert-Holle 1985).
Animal - mostly bird - dispersal of the fruits is very common in the family; Rhipsalis (see above for its distribution) has miseltoe-like fruits. In some Cactoideae in particular the seeds may germinate while still in the fruit, a form of vivipary (Cota-Sánchez et al. 2007).
Vegetative Variation. The stout, more or less succulent stem that characterises Cactaceae - even Pereskia has quite thick stems - results from primary or secondary thickening/expansion in the cortex, less often the pith (for which, see Troll & Rauh 1950; Boke 1954). There is considerable variation in growth form in the leafless Cactaceae, which range from often bizarrely-branched trees to tall and unbranched to flat-discoid to tussock-forming to stoloniferous ("Wandersprosse", Creeping Devils) and occasionally even rhizomatous plants (see e.g. Rauh 1979), and this is discussed in a phylogenetic context by Hernández-Hernández et al. (2011).
In Opuntioideae, the leaves of Pereskiopsis are large, petiolate, bifacial and more or less persistent, those of Quiabentia (the two may be sister taxa - e.g. Butterworth & Evans 2008) are terete, unifacial but also persistent; within Opuntioideae, taxa with leaves are derived (Griffith 2009). In most other Opuntioideae the leaves are small, terete and deciduous. Pereskia and Rhodocactus have leaves similar to those of Pereskiopsis. The more ordinary-appearing leaf types in Opuntioideae are probably derived more than once (e.g. Griffith & Porter 2009; Ritz et al. 2012), and those of Pereskia s.l., although similar, represent the plesiomorphic condition for the family (but c.f. Griffith 2004, 2008). Complicating the issue is the restriction of stomata to leaves and the stem adjacent to areoles in leafy Opuntioideae (Griffith 2008). One commonly thinks of Cactoideae in particular as being leafless, but Mauseth (2007) showed that most do have leaves, although they are up to only 1.5(-2.5) mm long when mature and so are mostly shorter than the terete leaves of Opuntioideae. Despite their small size, Cactoideae leaves may have a rudimentary lamina with vascular tissue, stomata, etc. The leaf base is early distinguishable from the rest of the leaf, and its subsequent development results in the ribs and tubercles along the stem that are characteristic of so many Cactaceae (Boke 1954).
The spines and hairs that make up the areoles of Cactaceae represent a short shoot, and short shoots may keep on growing and adding spines and even leaves, as in Pereskia. The multicellular hairs in the areoles, which sometimes cover the stem, are similar to those found in Anacampserotaceae, etc. Mammillaria has dimorphic areoles: There are normal spiny areoles born on tubercules (hence the generic name) and spineless areoles that bear flowers that are found in the axils of the tubercules; see also Rauh (1979) for inflorescence development.
Chemistry, Morphology, etc. The roots of at least some Cactoideae have an open type of apical meristem (Rodríguez-Rodríguez et al. 2003). Given the width of their stems, it is not surprising that many Cactaceae have very broad apical meristems 400-1500 µm across, rather broader than those of other flowering plants (Gifford 1954; Clowes 1961: sampling poor), although they can be rather narrower, 80-329 µm, in Pereskia in particular (Boke 1954). The cortex is particularly variable in Cactoideae. Mauseth and Landrum (1997) commented on the apparently very long-lived epidermis in many Cactaceae, which may remain functional for hundreds of years. Cuticle waxes in the form of spiral rodlets occur in Cereeae.
There is potentially interesting variation within the parallelocytic stomata "type" so common here. In both Pereskia and Opuntioideae the subsidiary cells do not, or only barely, overlap the ends of the guard cells, the "opuntioid" stomatal type (it could be called brachyparallelocytic!), whereas in other Cactaceae the subsidiary cells successively more broadly invest the poles of the whole stomatal apparatus. Wallace and Dickie (2002) note that the stomata of Opuntioideae are unique (see above). There is also variation in stomatal orientation. The stomata on the stems of Pereskia and Opuntioideae are oriented parallel to the long axis of the stem, while in Cactoideae they tend to be unoriented (Eggli 1984).
The inferior ovary of Cactaceae is a text-book example of receptacular epigyny with tissue investing the ovary being of axial origin (Boke 1964; see also Tiagi 1963 and references). Thus in genera like Opuntia areoles arranged in spirals cover the inferior ovary; it is as if the ovary had sunk into the stem. In Pereskia nemorosa and a few other Cactaceae flowers may arise from the axils of the leaves or from areoles on the ovary, the proliferating infliorescences in the characterization above (Rauh 1979; Leuenberger 2008). The hypanthium so conspicuous in some Cactoideae in particular is an elaboration of this axial tissue, although an obvious hypanthium may sometimes be absent. Tiagi (1963) that in Pereskia aculeata and P. sacharosa the course of the vascular tissue in the hypanthium was S-shaped, while in P. bleo and P. grandifolia it took the course of an inverted U; members of the first pair belong to both Pereskia clades. Vascularization of "prophylls", bracts and perianth members of the flowers varies (Tiagi 1963). The initial stages of androecial development may be as either separate, more or less spirally-arranged primordia, or a ring primordium (Leins & Erbar 1994b). Ovary placentation is variable. Placentae may alternate with septae, and/or be more or less basal; Leins and Schwitalla (1988) interpret the condition in which ovules are associated with incomplete septae proceeding from the ovary wall as the plesiomorphic condition for Cactaceae (see also Leins & Schwitalla 1986). However, the evolution of this inferior ovary needs to be re-examined given the paraphyly of Pereskia s.l. and the probable position of Portulacaceae as sister to Cactaceae; some species of Pereskia s. str. have superior ovaries (see Rauh 1979; Edwards et al. 2005).
The nucellus in Parodia may protrude through the micropyle (Rauh 1979). Cisneros et al. (2011) suggest that the inner integument of species of Hylocereus may be 4-5 cells across, but this is not readily to be seen in the images they provide.
For general information, see Barthlott and Hunt (1993), Anderson (2001) and Nobel (2002), as well as Hunt et al. (2006) for an excellent summary of the family, including a volume of superb photographs of nearly all species taken mostly in the wild. For Pereskia s.l., see Neumann (1935: pollen, etc., development), Leuenberger (1986: general), and Mauseth and Landrum (1997: "relictual" anatomical characters). For Opuntioideae, see Hunt and Taylor (2002: general) and Stuppy (2002: see morphology); for general anatomy see Mauseth (2005), for wood anatomy, see Mauseth (2006c). For ovules, etc., see Mauritzon (1934d) and Maheshwari & Chopra (1955), for chemistry, see Hegnauer (1964, 1989), for spines, see Schlegel (2009 and literature, morphology and structure), for pollen, see Leuenberger (1976: general) and Garralla and Cuadrado (2007: Opuntioideae), for seed morphology, see Barthlott and Voigt (1979), for that of Cactoideae, see Barthlott and Hunt (2000), for general anatomy, see Terrazas and Arias (2003: esp. Cactoideae), for some pollen, see Cuadrado and Garralla (2009), for floral morphology, see Ross (1982), for wide-band tracheids in particular, see Mauseth (2004), Godofredo and Melo-de-Pinna (2008) and Arruda and Melo-de-Pinna (2010), and for structure-function relationships, see Mauseth (2006a). For Maiheunia some information is taken from Gibson (1977: anatomy), Mauseth (1999: anatomy), and Leuenberger (1997: general); Taylor (2005) is a good introduction.
Phylogeny. The basic phylogenetic relationships within Cactaceae are perhaps still rather uncertain, with chloroplast and nuclear genes sometimes suggesting different major clades (see Butterworth 2006a and Nyffeler & Eggli 2010a for summaries). A study by Nyffeler (2002) found rather weak support for the subfamilies and that perhaps rather distressingly Pereskia was not clearly monophyletic. Edwards et al. (2005) confirmed that Pereskia s.l. was paraphyletic, which allowed them to shed new light on the evolution of the cactus habit (c.f. Butterworth & Wallace 2005 - topology different). For more details on the relationships of the major clades in Cactaceae, now all individually quite well supported, see Butterworth and Edwards (2008), Hernández-Hernández et al. (2011: position of Maihuenoideae unclear) and especially Arakaki et al. (2011); details of relationships in Bárcenas et al. (2011) were rather unclear, but only the trnK-matK region was examined. Vázquez-Sánchez et al. (2013) discussed the phylogeny of Cacteae.
For relationships within Opuntioideae, see Griffith (2002), Wallace and Dickie (2002), Butterworth and Edwards (2008), Hernández-Hernández et al. (2011) and especially Griffith and Porter (2009). The latter found the well-supported set of relationships [Maihueniopsis et al. [Pterocactus [terete-stemmed species + flat-stemmed species]]]; the leafy Pereskiopsis is in a derived position in the clade (c.f. e.g. Mauseth 2005 on its apparently plesiomorphous features). Ritz et al. (2012) examined the phylogeny and evolution of Andean species of Opuntia with terete stems.
Within Cactoideae, the distinctive Blossfeldia liliputana (= Blossfeldioideae Crozier) is sister to all other Cactoideae (Crozier 2004), and although there was initially some controversy over this position, it has been confirmed (e.g. Gorelick 2004; Mauseth 2006b; Butterworth 2006b; Arakaki et al. 2011). Hernández-Hernández et al. (2011) provide a quite detailed phylogeny of Cactoideae, although for the most part maximum likelihood bootstraps were low and maximum parsimony support still lower; earlier studies of Cacteae (Butterworth et al. 2002) and Mammillaria (Butterworth & Wallace 2004) faced the same problem. For the phylogeny and evolution of South American mountain cacti, see Ritz et al. (2007), for that of Gymnocalycium, see Meregalli et al. (2010) and Demaio et al. (2011), for Pfeifferia and relatives, see Calvente et al. (2011), for Rhipsalidae, see Calvente et al. (2011a, b: also character evolution), for Echinopsis see Schlumpberger and Renner (2012), and for Rhipsalis, see Calvente (2012). See also Wallace and Cota (1996) for the rpoCI intron and Wallace and Gibson (2002) and Nyffeler and Eggli (2010) for general relationships.
Classification. Metzing and Kiesling (2008) summarize early (pre-DNA) studies in the family, and include reproductions of some remarkable evolutionary trees. For a recent classification of the whole family, genera in the tribes being listed, see Nyffeler and Eggli (2010a).
Over the years, there have been major disagreements over generic limits, and depending on the author, the number of genera occurring in the family varies by a factor of ten, and of the species by a factor of two. For example, in Cactoideae a mere sixteen genera included all the species in the subfamily in 1903, but now as many as 116 genera may be recognized (Hunt 2002). Bárcenas et al. (2011) sampled quite extensively in the family and found that many tribes and genera in both the big subfamilies were not monophyletic: Only 4/6 and 14/36 genera of Opuntioideae and Cactoideae respectively for which two or more species were sampled turned out to be monophyletic. Floral traits often reflect pollinator preferences rather than clades, and growth bait is also labile (Schlumpberger & Renner 2012: Echinopsis area). Much phylogenetic work explicitly or implicitly has taxonomic implications (e.g. Korotkova et al. 2010; Calvente et al. 2011; and especially Bárcenas et al. 2011). For generic limits in Cacteae, see Vázquez-Sánchez et al. (2013).
Opuntia has been broadly delmited, but Wallace and Dickie (2002) have suggested that it should be dismembered, with sixteen genera in Opuntioideae. The situation in Opuntioideae is indeed a mess, as is clear from the recent study by Griffith and Porter (2009). Hunt (1999, 2002) had earlier proposed the recognition of about eight broadly-delimited genera, roughly equivalent to tribes of other workers, which certainly makes sense pending sorting out the phylogeny of the group as a whole - and might also be a sensible final solution. Whether or not the stakeholders (Griffith & Porter 2009) can agree might be another matter.
For revisions of critical taxa, see work by Leuenberger, e.g. Leuenberger and Eggli (1999: Blossfeldia) and Leuenberger (1986: Pereskia and Rhodocactus, 1997: Maiheunia, 2008: update on the literature of all three). Calvente (2012) enumerated the taxa in Rhipsalis.
Previous Relationships. Despite the distinctive appearance of the "leafless" cacti, the relationships of the family with other Caryophyllales has generaly been recognized.